diff --git a/.changelog/17426.txt b/.changelog/17426.txt
new file mode 100644
index 000000000..d8fbd2ae2
--- /dev/null
+++ b/.changelog/17426.txt
@@ -0,0 +1,5 @@
+```release-note:improvement
+ peering: gRPC queries for TrustBundleList, TrustBundleRead, PeeringList, and PeeringRead now support blocking semantics,
+ reducing network and CPU demand.
+ The HTTP APIs for Peering List and Read have been updated to support blocking.
+ ```
\ No newline at end of file
diff --git a/agent/blockingquery/blockingquery.go b/agent/blockingquery/blockingquery.go
new file mode 100644
index 000000000..cb4611022
--- /dev/null
+++ b/agent/blockingquery/blockingquery.go
@@ -0,0 +1,208 @@
+package blockingquery
+
+import (
+	"context"
+	"errors"
+	"fmt"
+	"time"
+
+	"github.com/armon/go-metrics"
+	"github.com/hashicorp/go-memdb"
+
+	"github.com/hashicorp/consul/agent/consul/state"
+	"github.com/hashicorp/consul/lib"
+)
+
+// Sentinel errors that must be used with blockingQuery
+var (
+	ErrNotFound   = fmt.Errorf("no data found for query")
+	ErrNotChanged = fmt.Errorf("data did not change for query")
+)
+
+// QueryFn is used to perform a query operation. See Server.blockingQuery for
+// the requirements of this function.
+type QueryFn func(memdb.WatchSet, *state.Store) error
+
+// RequestOptions are options used by Server.blockingQuery to modify the
+// behaviour of the query operation, or to populate response metadata.
+type RequestOptions interface {
+	GetToken() string
+	GetMinQueryIndex() uint64
+	GetMaxQueryTime() (time.Duration, error)
+	GetRequireConsistent() bool
+}
+
+// ResponseMeta is an interface used to populate the response struct
+// with metadata about the query and the state of the server.
+type ResponseMeta interface {
+	SetLastContact(time.Duration)
+	SetKnownLeader(bool)
+	GetIndex() uint64
+	SetIndex(uint64)
+	SetResultsFilteredByACLs(bool)
+}
+
+// FSMServer is interface into the stateful components of a Consul server, such
+// as memdb or raft leadership.
+type FSMServer interface {
+	ConsistentRead() error
+	DecrementBlockingQueries() uint64
+	GetShutdownChannel() chan struct{}
+	GetState() *state.Store
+	IncrementBlockingQueries() uint64
+	RPCQueryTimeout(time.Duration) time.Duration
+	SetQueryMeta(ResponseMeta, string)
+}
+
+// Query performs a blocking query if opts.GetMinQueryIndex is
+// greater than 0, otherwise performs a non-blocking query. Blocking queries will
+// block until responseMeta.Index is greater than opts.GetMinQueryIndex,
+// or opts.GetMaxQueryTime is reached. Non-blocking queries return immediately
+// after performing the query.
+//
+// If opts.GetRequireConsistent is true, blockingQuery will first verify it is
+// still the cluster leader before performing the query.
+//
+// The query function is expected to be a closure that has access to responseMeta
+// so that it can set the Index. The actual result of the query is opaque to blockingQuery.
+//
+// The query function can return ErrNotFound, which is a sentinel error. Returning
+// ErrNotFound indicates that the query found no results, which allows
+// blockingQuery to keep blocking until the query returns a non-nil error.
+// The query function must take care to set the actual result of the query to
+// nil in these cases, otherwise when blockingQuery times out it may return
+// a previous result. ErrNotFound will never be returned to the caller, it is
+// converted to nil before returning.
+//
+// The query function can return ErrNotChanged, which is a sentinel error. This
+// can only be returned on calls AFTER the first call, as it would not be
+// possible to detect the absence of a change on the first call. Returning
+// ErrNotChanged indicates that the query results are identical to the prior
+// results which allows blockingQuery to keep blocking until the query returns
+// a real changed result.
+//
+// The query function must take care to ensure the actual result of the query
+// is either left unmodified or explicitly left in a good state before
+// returning, otherwise when blockingQuery times out it may return an
+// incomplete or unexpected result. ErrNotChanged will never be returned to the
+// caller, it is converted to nil before returning.
+//
+// If query function returns any other error, the error is returned to the caller
+// immediately.
+//
+// The query function must follow these rules:
+//
+//  1. to access data it must use the passed in state.Store.
+//  2. it must set the responseMeta.Index to an index greater than
+//     opts.GetMinQueryIndex if the results return by the query have changed.
+//  3. any channels added to the memdb.WatchSet must unblock when the results
+//     returned by the query have changed.
+//
+// To ensure optimal performance of the query, the query function should make a
+// best-effort attempt to follow these guidelines:
+//
+//  1. only set responseMeta.Index to an index greater than
+//     opts.GetMinQueryIndex when the results returned by the query have changed.
+//  2. any channels added to the memdb.WatchSet should only unblock when the
+//     results returned by the query have changed.
+func Query(
+	fsmServer FSMServer,
+	requestOpts RequestOptions,
+	responseMeta ResponseMeta,
+	query QueryFn,
+) error {
+	var ctx context.Context = &lib.StopChannelContext{StopCh: fsmServer.GetShutdownChannel()}
+
+	metrics.IncrCounter([]string{"rpc", "query"}, 1)
+
+	minQueryIndex := requestOpts.GetMinQueryIndex()
+	// Perform a non-blocking query
+	if minQueryIndex == 0 {
+		if requestOpts.GetRequireConsistent() {
+			if err := fsmServer.ConsistentRead(); err != nil {
+				return err
+			}
+		}
+
+		var ws memdb.WatchSet
+		err := query(ws, fsmServer.GetState())
+		fsmServer.SetQueryMeta(responseMeta, requestOpts.GetToken())
+		if errors.Is(err, ErrNotFound) || errors.Is(err, ErrNotChanged) {
+			return nil
+		}
+		return err
+	}
+
+	maxQueryTimeout, err := requestOpts.GetMaxQueryTime()
+	if err != nil {
+		return err
+	}
+	timeout := fsmServer.RPCQueryTimeout(maxQueryTimeout)
+	ctx, cancel := context.WithTimeout(ctx, timeout)
+	defer cancel()
+
+	count := fsmServer.IncrementBlockingQueries()
+	metrics.SetGauge([]string{"rpc", "queries_blocking"}, float32(count))
+	// decrement the count when the function returns.
+	defer fsmServer.DecrementBlockingQueries()
+
+	var (
+		notFound bool
+		ranOnce  bool
+	)
+
+	for {
+		if requestOpts.GetRequireConsistent() {
+			if err := fsmServer.ConsistentRead(); err != nil {
+				return err
+			}
+		}
+
+		// Operate on a consistent set of state. This makes sure that the
+		// abandon channel goes with the state that the caller is using to
+		// build watches.
+		store := fsmServer.GetState()
+
+		ws := memdb.NewWatchSet()
+		// This channel will be closed if a snapshot is restored and the
+		// whole state store is abandoned.
+		ws.Add(store.AbandonCh())
+
+		err := query(ws, store)
+		fsmServer.SetQueryMeta(responseMeta, requestOpts.GetToken())
+
+		switch {
+		case errors.Is(err, ErrNotFound):
+			if notFound {
+				// query result has not changed
+				minQueryIndex = responseMeta.GetIndex()
+			}
+			notFound = true
+		case errors.Is(err, ErrNotChanged):
+			if ranOnce {
+				// query result has not changed
+				minQueryIndex = responseMeta.GetIndex()
+			}
+		case err != nil:
+			return err
+		}
+		ranOnce = true
+
+		if responseMeta.GetIndex() > minQueryIndex {
+			return nil
+		}
+
+		// block until something changes, or the timeout
+		if err := ws.WatchCtx(ctx); err != nil {
+			// exit if we've reached the timeout, or other cancellation
+			return nil
+		}
+
+		// exit if the state store has been abandoned
+		select {
+		case <-store.AbandonCh():
+			return nil
+		default:
+		}
+	}
+}
diff --git a/agent/blockingquery/blockingquery_test.go b/agent/blockingquery/blockingquery_test.go
new file mode 100644
index 000000000..6cfc07c11
--- /dev/null
+++ b/agent/blockingquery/blockingquery_test.go
@@ -0,0 +1,4 @@
+package blockingquery
+
+// TODO: move tests from the consul package, rpc_test.go, TestServer_blockingQuery
+// here using mock for FSMServer w/ structs.QueryOptions and structs.QueryOptions
diff --git a/agent/cache-types/peerings.go b/agent/cache-types/peerings.go
index 5a8e1a685..e72b43d56 100644
--- a/agent/cache-types/peerings.go
+++ b/agent/cache-types/peerings.go
@@ -7,22 +7,24 @@ import (
 	"context"
 	"fmt"
 	"strconv"
-	"time"
 
-	external "github.com/hashicorp/consul/agent/grpc-external"
-	"github.com/hashicorp/consul/proto/private/pbpeering"
 	"github.com/mitchellh/hashstructure"
 	"google.golang.org/grpc"
 	"google.golang.org/grpc/codes"
+	"google.golang.org/grpc/metadata"
 	"google.golang.org/grpc/status"
 
 	"github.com/hashicorp/consul/agent/cache"
+	external "github.com/hashicorp/consul/agent/grpc-external"
 	"github.com/hashicorp/consul/agent/structs"
+	"github.com/hashicorp/consul/proto/private/pbpeering"
 )
 
 // PeeringListName is the recommended name for registration.
 const PeeringListName = "peers"
 
+// PeeringListRequest represents the combination of request payload
+// and options that would normally be sent over headers.
 type PeeringListRequest struct {
 	Request *pbpeering.PeeringListRequest
 	structs.QueryOptions
@@ -32,13 +34,10 @@ func (r *PeeringListRequest) CacheInfo() cache.RequestInfo {
 	info := cache.RequestInfo{
 		Token:          r.Token,
 		Datacenter:     "",
-		MinIndex:       0,
-		Timeout:        0,
-		MustRevalidate: false,
-
-		// OPTIMIZE(peering): Cache.notifyPollingQuery polls at this interval. We need to revisit how that polling works.
-		//        	          Using an exponential backoff when the result hasn't changed may be preferable.
-		MaxAge: 1 * time.Second,
+		MinIndex:       r.MinQueryIndex,
+		Timeout:        r.MaxQueryTime,
+		MaxAge:         r.MaxAge,
+		MustRevalidate: r.MustRevalidate,
 	}
 
 	v, err := hashstructure.Hash([]interface{}{
@@ -56,7 +55,7 @@ func (r *PeeringListRequest) CacheInfo() cache.RequestInfo {
 
 // Peerings supports fetching the list of peers for a given partition or wildcard-specifier.
 type Peerings struct {
-	RegisterOptionsNoRefresh
+	RegisterOptionsBlockingRefresh
 	Client PeeringLister
 }
 
@@ -67,7 +66,7 @@ type PeeringLister interface {
 	) (*pbpeering.PeeringListResponse, error)
 }
 
-func (t *Peerings) Fetch(_ cache.FetchOptions, req cache.Request) (cache.FetchResult, error) {
+func (t *Peerings) Fetch(opts cache.FetchOptions, req cache.Request) (cache.FetchResult, error) {
 	var result cache.FetchResult
 
 	// The request should be a PeeringListRequest.
@@ -79,10 +78,17 @@ func (t *Peerings) Fetch(_ cache.FetchOptions, req cache.Request) (cache.FetchRe
 			"Internal cache failure: request wrong type: %T", req)
 	}
 
-	// Always allow stale - there's no point in hitting leader if the request is
-	// going to be served from cache and end up arbitrarily stale anyway. This
-	// allows cached service-discover to automatically read scale across all
-	// servers too.
+	// Lightweight copy this object so that manipulating QueryOptions doesn't race.
+	dup := *reqReal
+	reqReal = &dup
+
+	// Set the minimum query index to our current index, so we block
+	reqReal.QueryOptions.MinQueryIndex = opts.MinIndex
+	reqReal.QueryOptions.MaxQueryTime = opts.Timeout
+
+	// We allow stale queries here to spread out the RPC load, but peerstream information, including the STATUS,
+	// will not be returned. Right now this is fine for the watch in proxycfg/mesh_gateway.go,
+	// but it could be a problem for a future consumer.
 	reqReal.QueryOptions.SetAllowStale(true)
 
 	ctx, err := external.ContextWithQueryOptions(context.Background(), reqReal.QueryOptions)
@@ -91,7 +97,8 @@ func (t *Peerings) Fetch(_ cache.FetchOptions, req cache.Request) (cache.FetchRe
 	}
 
 	// Fetch
-	reply, err := t.Client.PeeringList(ctx, reqReal.Request)
+	var header metadata.MD
+	reply, err := t.Client.PeeringList(ctx, reqReal.Request, grpc.Header(&header))
 	if err != nil {
 		// Return an empty result if the error is due to peering being disabled.
 		// This allows mesh gateways to receive an update and confirm that the watch is set.
@@ -103,8 +110,19 @@ func (t *Peerings) Fetch(_ cache.FetchOptions, req cache.Request) (cache.FetchRe
 		return result, err
 	}
 
+	// This first case is using the legacy index field
+	// It should be removed in a future version in favor of the index from QueryMeta
+	if reply.OBSOLETE_Index != 0 {
+		result.Index = reply.OBSOLETE_Index
+	} else {
+		meta, err := external.QueryMetaFromGRPCMeta(header)
+		if err != nil {
+			return result, fmt.Errorf("could not convert gRPC metadata to query meta: %w", err)
+		}
+		result.Index = meta.GetIndex()
+	}
+
 	result.Value = reply
-	result.Index = reply.Index
 
 	return result, nil
 }
diff --git a/agent/cache-types/peerings_test.go b/agent/cache-types/peerings_test.go
index 954addfe5..75fc21371 100644
--- a/agent/cache-types/peerings_test.go
+++ b/agent/cache-types/peerings_test.go
@@ -8,14 +8,16 @@ import (
 	"testing"
 	"time"
 
-	"github.com/mitchellh/copystructure"
 	"github.com/stretchr/testify/mock"
 	"github.com/stretchr/testify/require"
 	"google.golang.org/grpc"
 	"google.golang.org/grpc/codes"
+	"google.golang.org/grpc/metadata"
 	grpcstatus "google.golang.org/grpc/status"
 
 	"github.com/hashicorp/consul/agent/cache"
+	external "github.com/hashicorp/consul/agent/grpc-external"
+	"github.com/hashicorp/consul/agent/structs"
 	"github.com/hashicorp/consul/proto/private/pbpeering"
 )
 
@@ -24,7 +26,6 @@ func TestPeerings(t *testing.T) {
 	typ := &Peerings{Client: client}
 
 	resp := &pbpeering.PeeringListResponse{
-		Index: 48,
 		Peerings: []*pbpeering.Peering{
 			{
 				Name:                "peer1",
@@ -36,12 +37,38 @@ func TestPeerings(t *testing.T) {
 	}
 
 	// Expect the proper call.
-	// This also returns the canned response above.
-	client.On("PeeringList", mock.Anything, mock.Anything).
-		Return(resp, nil)
+	// This also set the gRPC metadata returned by pointer.
+	client.On("PeeringList", mock.Anything, mock.Anything, mock.Anything).
+		Return(resp, nil).
+		Run(func(args mock.Arguments) {
+			// Validate Query Options
+			ctx := args.Get(0).(context.Context)
+			out, ok := metadata.FromOutgoingContext(ctx)
+			require.True(t, ok)
+			ctx = metadata.NewIncomingContext(ctx, out)
+
+			options, err := external.QueryOptionsFromContext(ctx)
+			require.NoError(t, err)
+			require.Equal(t, uint64(28), options.MinQueryIndex)
+			require.Equal(t, time.Duration(1100), options.MaxQueryTime)
+			require.True(t, options.AllowStale)
+
+			// Send back Query Meta on pointer of header
+			header := args.Get(2).(grpc.HeaderCallOption)
+			qm := structs.QueryMeta{
+				Index: 48,
+			}
+
+			md, err := external.GRPCMetadataFromQueryMeta(qm)
+			require.NoError(t, err)
+			*header.HeaderAddr = md
+		})
 
 	// Fetch and assert against the result.
-	result, err := typ.Fetch(cache.FetchOptions{}, &PeeringListRequest{
+	result, err := typ.Fetch(cache.FetchOptions{
+		MinIndex: 28,
+		Timeout:  time.Duration(1100),
+	}, &PeeringListRequest{
 		Request: &pbpeering.PeeringListRequest{},
 	})
 	require.NoError(t, err)
@@ -58,7 +85,7 @@ func TestPeerings_PeeringDisabled(t *testing.T) {
 	var resp *pbpeering.PeeringListResponse
 
 	// Expect the proper call, but return the peering disabled error
-	client.On("PeeringList", mock.Anything, mock.Anything).
+	client.On("PeeringList", mock.Anything, mock.Anything, mock.Anything).
 		Return(resp, grpcstatus.Error(codes.FailedPrecondition, "peering must be enabled to use this endpoint"))
 
 	// Fetch and assert against the result.
@@ -81,54 +108,3 @@ func TestPeerings_badReqType(t *testing.T) {
 	require.Error(t, err)
 	require.Contains(t, err.Error(), "wrong type")
 }
-
-// This test asserts that we can continuously poll this cache type, given that it doesn't support blocking.
-func TestPeerings_MultipleUpdates(t *testing.T) {
-	c := cache.New(cache.Options{})
-
-	client := NewMockPeeringLister(t)
-
-	// On each mock client call to PeeringList we will increment the index by 1
-	// to simulate new data arriving.
-	resp := &pbpeering.PeeringListResponse{
-		Index: uint64(0),
-	}
-
-	client.On("PeeringList", mock.Anything, mock.Anything).
-		Return(func(ctx context.Context, in *pbpeering.PeeringListRequest, opts ...grpc.CallOption) *pbpeering.PeeringListResponse {
-			resp.Index++
-			// Avoids triggering the race detection by copying the output
-			copyResp, err := copystructure.Copy(resp)
-			require.NoError(t, err)
-			output := copyResp.(*pbpeering.PeeringListResponse)
-			return output
-		}, nil)
-
-	c.RegisterType(PeeringListName, &Peerings{Client: client})
-
-	ch := make(chan cache.UpdateEvent)
-	ctx, cancel := context.WithTimeout(context.Background(), 5*time.Second)
-	t.Cleanup(cancel)
-
-	require.NoError(t, c.Notify(ctx, PeeringListName, &PeeringListRequest{
-		Request: &pbpeering.PeeringListRequest{},
-	}, "updates", ch))
-
-	i := uint64(1)
-	for {
-		select {
-		case <-ctx.Done():
-			t.Fatal("context deadline exceeded")
-			return
-		case update := <-ch:
-			// Expect to receive updates for increasing indexes serially.
-			actual := update.Result.(*pbpeering.PeeringListResponse)
-			require.Equal(t, i, actual.Index)
-			i++
-
-			if i > 3 {
-				return
-			}
-		}
-	}
-}
diff --git a/agent/cache-types/trust_bundle.go b/agent/cache-types/trust_bundle.go
index fda4cd958..301b18977 100644
--- a/agent/cache-types/trust_bundle.go
+++ b/agent/cache-types/trust_bundle.go
@@ -7,10 +7,10 @@ import (
 	"context"
 	"fmt"
 	"strconv"
-	"time"
 
 	"github.com/mitchellh/hashstructure"
 	"google.golang.org/grpc"
+	"google.golang.org/grpc/metadata"
 
 	"github.com/hashicorp/consul/agent/cache"
 	external "github.com/hashicorp/consul/agent/grpc-external"
@@ -21,6 +21,8 @@ import (
 // Recommended name for registration.
 const TrustBundleReadName = "peer-trust-bundle"
 
+// TrustBundleReadRequest represents the combination of request payload
+// and options that would normally be sent over headers.
 type TrustBundleReadRequest struct {
 	Request *pbpeering.TrustBundleReadRequest
 	structs.QueryOptions
@@ -30,13 +32,10 @@ func (r *TrustBundleReadRequest) CacheInfo() cache.RequestInfo {
 	info := cache.RequestInfo{
 		Token:          r.Token,
 		Datacenter:     "",
-		MinIndex:       0,
-		Timeout:        0,
-		MustRevalidate: false,
-
-		// OPTIMIZE(peering): Cache.notifyPollingQuery polls at this interval. We need to revisit how that polling works.
-		//        	          Using an exponential backoff when the result hasn't changed may be preferable.
-		MaxAge: 1 * time.Second,
+		MinIndex:       r.MinQueryIndex,
+		Timeout:        r.MaxQueryTime,
+		MaxAge:         r.MaxAge,
+		MustRevalidate: r.MustRevalidate,
 	}
 
 	v, err := hashstructure.Hash([]interface{}{
@@ -56,7 +55,7 @@ func (r *TrustBundleReadRequest) CacheInfo() cache.RequestInfo {
 // TrustBundle supports fetching discovering service instances via prepared
 // queries.
 type TrustBundle struct {
-	RegisterOptionsNoRefresh
+	RegisterOptionsBlockingRefresh
 	Client TrustBundleReader
 }
 
@@ -67,7 +66,7 @@ type TrustBundleReader interface {
 	) (*pbpeering.TrustBundleReadResponse, error)
 }
 
-func (t *TrustBundle) Fetch(_ cache.FetchOptions, req cache.Request) (cache.FetchResult, error) {
+func (t *TrustBundle) Fetch(opts cache.FetchOptions, req cache.Request) (cache.FetchResult, error) {
 	var result cache.FetchResult
 
 	// The request should be a TrustBundleReadRequest.
@@ -79,6 +78,14 @@ func (t *TrustBundle) Fetch(_ cache.FetchOptions, req cache.Request) (cache.Fetc
 			"Internal cache failure: request wrong type: %T", req)
 	}
 
+	// Lightweight copy this object so that manipulating QueryOptions doesn't race.
+	dup := *reqReal
+	reqReal = &dup
+
+	// Set the minimum query index to our current index, so we block
+	reqReal.QueryOptions.MinQueryIndex = opts.MinIndex
+	reqReal.QueryOptions.MaxQueryTime = opts.Timeout
+
 	// Always allow stale - there's no point in hitting leader if the request is
 	// going to be served from cache and end up arbitrarily stale anyway. This
 	// allows cached service-discover to automatically read scale across all
@@ -91,13 +98,25 @@ func (t *TrustBundle) Fetch(_ cache.FetchOptions, req cache.Request) (cache.Fetc
 		return result, err
 	}
 
-	reply, err := t.Client.TrustBundleRead(ctx, reqReal.Request)
+	var header metadata.MD
+	reply, err := t.Client.TrustBundleRead(ctx, reqReal.Request, grpc.Header(&header))
 	if err != nil {
 		return result, err
 	}
 
+	// This first case is using the legacy index field
+	// It should be removed in a future version in favor of the index from QueryMeta
+	if reply.OBSOLETE_Index != 0 {
+		result.Index = reply.OBSOLETE_Index
+	} else {
+		meta, err := external.QueryMetaFromGRPCMeta(header)
+		if err != nil {
+			return result, fmt.Errorf("could not convert gRPC metadata to query meta: %w", err)
+		}
+		result.Index = meta.GetIndex()
+	}
+
 	result.Value = reply
-	result.Index = reply.Index
 
 	return result, nil
 }
diff --git a/agent/cache-types/trust_bundle_test.go b/agent/cache-types/trust_bundle_test.go
index 67df2496c..dc39c3555 100644
--- a/agent/cache-types/trust_bundle_test.go
+++ b/agent/cache-types/trust_bundle_test.go
@@ -10,8 +10,12 @@ import (
 
 	"github.com/stretchr/testify/mock"
 	"github.com/stretchr/testify/require"
+	"google.golang.org/grpc"
+	"google.golang.org/grpc/metadata"
 
 	"github.com/hashicorp/consul/agent/cache"
+	external "github.com/hashicorp/consul/agent/grpc-external"
+	"github.com/hashicorp/consul/agent/structs"
 	"github.com/hashicorp/consul/proto/private/pbpeering"
 )
 
@@ -20,7 +24,6 @@ func TestTrustBundle(t *testing.T) {
 	typ := &TrustBundle{Client: client}
 
 	resp := &pbpeering.TrustBundleReadResponse{
-		Index: 48,
 		Bundle: &pbpeering.PeeringTrustBundle{
 			PeerName: "peer1",
 			RootPEMs: []string{"peer1-roots"},
@@ -29,15 +32,41 @@ func TestTrustBundle(t *testing.T) {
 
 	// Expect the proper call.
 	// This also returns the canned response above.
-	client.On("TrustBundleRead", mock.Anything, mock.Anything).
+	client.On("TrustBundleRead", mock.Anything, mock.Anything, mock.Anything).
 		Run(func(args mock.Arguments) {
+			// Validate Query Options
+			ctx := args.Get(0).(context.Context)
+			out, ok := metadata.FromOutgoingContext(ctx)
+			require.True(t, ok)
+			ctx = metadata.NewIncomingContext(ctx, out)
+
+			options, err := external.QueryOptionsFromContext(ctx)
+			require.NoError(t, err)
+			require.Equal(t, uint64(28), options.MinQueryIndex)
+			require.Equal(t, time.Duration(1100), options.MaxQueryTime)
+			require.True(t, options.AllowStale)
+
+			// Validate Request
 			req := args.Get(1).(*pbpeering.TrustBundleReadRequest)
 			require.Equal(t, "foo", req.Name)
+
+			// Send back Query Meta on pointer of header
+			header := args.Get(2).(grpc.HeaderCallOption)
+			qm := structs.QueryMeta{
+				Index: 48,
+			}
+
+			md, err := external.GRPCMetadataFromQueryMeta(qm)
+			require.NoError(t, err)
+			*header.HeaderAddr = md
 		}).
 		Return(resp, nil)
 
 	// Fetch and assert against the result.
-	result, err := typ.Fetch(cache.FetchOptions{}, &TrustBundleReadRequest{
+	result, err := typ.Fetch(cache.FetchOptions{
+		MinIndex: 28,
+		Timeout:  time.Duration(1100),
+	}, &TrustBundleReadRequest{
 		Request: &pbpeering.TrustBundleReadRequest{
 			Name: "foo",
 		},
@@ -59,55 +88,3 @@ func TestTrustBundle_badReqType(t *testing.T) {
 	require.Error(t, err)
 	require.Contains(t, err.Error(), "wrong type")
 }
-
-// This test asserts that we can continuously poll this cache type, given that it doesn't support blocking.
-func TestTrustBundle_MultipleUpdates(t *testing.T) {
-	c := cache.New(cache.Options{})
-
-	client := NewMockTrustBundleReader(t)
-
-	// On each mock client call to TrustBundleList by service we will increment the index by 1
-	// to simulate new data arriving.
-	resp := &pbpeering.TrustBundleReadResponse{
-		Index: uint64(0),
-	}
-
-	client.On("TrustBundleRead", mock.Anything, mock.Anything).
-		Run(func(args mock.Arguments) {
-			req := args.Get(1).(*pbpeering.TrustBundleReadRequest)
-			require.Equal(t, "foo", req.Name)
-
-			// Increment on each call.
-			resp.Index++
-		}).
-		Return(resp, nil)
-
-	c.RegisterType(TrustBundleReadName, &TrustBundle{Client: client})
-
-	ch := make(chan cache.UpdateEvent)
-	ctx, cancel := context.WithTimeout(context.Background(), 5*time.Second)
-	t.Cleanup(cancel)
-
-	err := c.Notify(ctx, TrustBundleReadName, &TrustBundleReadRequest{
-		Request: &pbpeering.TrustBundleReadRequest{Name: "foo"},
-	}, "updates", ch)
-	require.NoError(t, err)
-
-	i := uint64(1)
-	for {
-		select {
-		case <-ctx.Done():
-			t.Fatal("context deadline exceeded")
-			return
-		case update := <-ch:
-			// Expect to receive updates for increasing indexes serially.
-			actual := update.Result.(*pbpeering.TrustBundleReadResponse)
-			require.Equal(t, i, actual.Index)
-			i++
-
-			if i > 3 {
-				return
-			}
-		}
-	}
-}
diff --git a/agent/cache-types/trust_bundles.go b/agent/cache-types/trust_bundles.go
index a123145a4..a485ee534 100644
--- a/agent/cache-types/trust_bundles.go
+++ b/agent/cache-types/trust_bundles.go
@@ -7,11 +7,11 @@ import (
 	"context"
 	"fmt"
 	"strconv"
-	"time"
 
 	"github.com/mitchellh/hashstructure"
 	"google.golang.org/grpc"
 	"google.golang.org/grpc/codes"
+	"google.golang.org/grpc/metadata"
 	"google.golang.org/grpc/status"
 
 	"github.com/hashicorp/consul/agent/cache"
@@ -23,6 +23,8 @@ import (
 // Recommended name for registration.
 const TrustBundleListName = "trust-bundles"
 
+// TrustBundleListRequest represents the combination of request payload
+// and options that would normally be sent over headers.
 type TrustBundleListRequest struct {
 	Request *pbpeering.TrustBundleListByServiceRequest
 	structs.QueryOptions
@@ -32,13 +34,10 @@ func (r *TrustBundleListRequest) CacheInfo() cache.RequestInfo {
 	info := cache.RequestInfo{
 		Token:          r.Token,
 		Datacenter:     "",
-		MinIndex:       0,
-		Timeout:        0,
-		MustRevalidate: false,
-
-		// OPTIMIZE(peering): Cache.notifyPollingQuery polls at this interval. We need to revisit how that polling works.
-		//        	          Using an exponential backoff when the result hasn't changed may be preferable.
-		MaxAge: 1 * time.Second,
+		MinIndex:       r.MinQueryIndex,
+		Timeout:        r.MaxQueryTime,
+		MaxAge:         r.MaxAge,
+		MustRevalidate: r.MustRevalidate,
 	}
 
 	v, err := hashstructure.Hash([]interface{}{
@@ -60,7 +59,7 @@ func (r *TrustBundleListRequest) CacheInfo() cache.RequestInfo {
 // TrustBundles supports fetching discovering service instances via prepared
 // queries.
 type TrustBundles struct {
-	RegisterOptionsNoRefresh
+	RegisterOptionsBlockingRefresh
 	Client TrustBundleLister
 }
 
@@ -71,7 +70,7 @@ type TrustBundleLister interface {
 	) (*pbpeering.TrustBundleListByServiceResponse, error)
 }
 
-func (t *TrustBundles) Fetch(_ cache.FetchOptions, req cache.Request) (cache.FetchResult, error) {
+func (t *TrustBundles) Fetch(opts cache.FetchOptions, req cache.Request) (cache.FetchResult, error) {
 	var result cache.FetchResult
 
 	// The request should be a TrustBundleListRequest.
@@ -83,6 +82,14 @@ func (t *TrustBundles) Fetch(_ cache.FetchOptions, req cache.Request) (cache.Fet
 			"Internal cache failure: request wrong type: %T", req)
 	}
 
+	// Lightweight copy this object so that manipulating QueryOptions doesn't race.
+	dup := *reqReal
+	reqReal = &dup
+
+	// Set the minimum query index to our current index, so we block
+	reqReal.QueryOptions.MinQueryIndex = opts.MinIndex
+	reqReal.QueryOptions.MaxQueryTime = opts.Timeout
+
 	// Always allow stale - there's no point in hitting leader if the request is
 	// going to be served from cache and end up arbitrarily stale anyway. This
 	// allows cached service-discover to automatically read scale across all
@@ -95,20 +102,32 @@ func (t *TrustBundles) Fetch(_ cache.FetchOptions, req cache.Request) (cache.Fet
 		return result, err
 	}
 
-	reply, err := t.Client.TrustBundleListByService(ctx, reqReal.Request)
+	var header metadata.MD
+	reply, err := t.Client.TrustBundleListByService(ctx, reqReal.Request, grpc.Header(&header))
 	if err != nil {
 		// Return an empty result if the error is due to peering being disabled.
 		// This allows mesh gateways to receive an update and confirm that the watch is set.
 		if e, ok := status.FromError(err); ok && e.Code() == codes.FailedPrecondition {
 			result.Index = 1
-			result.Value = &pbpeering.TrustBundleListByServiceResponse{Index: 1}
+			result.Value = &pbpeering.TrustBundleListByServiceResponse{OBSOLETE_Index: 1}
 			return result, nil
 		}
 		return result, err
 	}
 
+	// This first case is using the legacy index field
+	// It should be removed in a future version in favor of the index from QueryMeta
+	if reply.OBSOLETE_Index != 0 {
+		result.Index = reply.OBSOLETE_Index
+	} else {
+		meta, err := external.QueryMetaFromGRPCMeta(header)
+		if err != nil {
+			return result, fmt.Errorf("could not convert gRPC metadata to query meta: %w", err)
+		}
+		result.Index = meta.GetIndex()
+	}
+
 	result.Value = reply
-	result.Index = reply.Index
 
 	return result, nil
 }
diff --git a/agent/cache-types/trust_bundles_test.go b/agent/cache-types/trust_bundles_test.go
index 861beed2f..373ba2a8d 100644
--- a/agent/cache-types/trust_bundles_test.go
+++ b/agent/cache-types/trust_bundles_test.go
@@ -10,10 +10,14 @@ import (
 
 	"github.com/stretchr/testify/mock"
 	"github.com/stretchr/testify/require"
+	"google.golang.org/grpc"
 	"google.golang.org/grpc/codes"
+	"google.golang.org/grpc/metadata"
 	grpcstatus "google.golang.org/grpc/status"
 
 	"github.com/hashicorp/consul/agent/cache"
+	external "github.com/hashicorp/consul/agent/grpc-external"
+	"github.com/hashicorp/consul/agent/structs"
 	"github.com/hashicorp/consul/proto/private/pbpeering"
 )
 
@@ -22,7 +26,6 @@ func TestTrustBundles(t *testing.T) {
 	typ := &TrustBundles{Client: client}
 
 	resp := &pbpeering.TrustBundleListByServiceResponse{
-		Index: 48,
 		Bundles: []*pbpeering.PeeringTrustBundle{
 			{
 				PeerName: "peer1",
@@ -33,15 +36,41 @@ func TestTrustBundles(t *testing.T) {
 
 	// Expect the proper call.
 	// This also returns the canned response above.
-	client.On("TrustBundleListByService", mock.Anything, mock.Anything).
+	client.On("TrustBundleListByService", mock.Anything, mock.Anything, mock.Anything).
 		Run(func(args mock.Arguments) {
+			// Validate Query Options
+			ctx := args.Get(0).(context.Context)
+			out, ok := metadata.FromOutgoingContext(ctx)
+			require.True(t, ok)
+			ctx = metadata.NewIncomingContext(ctx, out)
+
+			options, err := external.QueryOptionsFromContext(ctx)
+			require.NoError(t, err)
+			require.Equal(t, uint64(28), options.MinQueryIndex)
+			require.Equal(t, time.Duration(1100), options.MaxQueryTime)
+			require.True(t, options.AllowStale)
+
+			// Validate Request
 			req := args.Get(1).(*pbpeering.TrustBundleListByServiceRequest)
 			require.Equal(t, "foo", req.ServiceName)
+
+			// Send back Query Meta on pointer of header
+			header := args.Get(2).(grpc.HeaderCallOption)
+			qm := structs.QueryMeta{
+				Index: 48,
+			}
+
+			md, err := external.GRPCMetadataFromQueryMeta(qm)
+			require.NoError(t, err)
+			*header.HeaderAddr = md
 		}).
 		Return(resp, nil)
 
 	// Fetch and assert against the result.
-	result, err := typ.Fetch(cache.FetchOptions{}, &TrustBundleListRequest{
+	result, err := typ.Fetch(cache.FetchOptions{
+		MinIndex: 28,
+		Timeout:  time.Duration(1100),
+	}, &TrustBundleListRequest{
 		Request: &pbpeering.TrustBundleListByServiceRequest{
 			ServiceName: "foo",
 		},
@@ -61,7 +90,7 @@ func TestTrustBundles_PeeringDisabled(t *testing.T) {
 
 	// Expect the proper call.
 	// This also returns the canned response above.
-	client.On("TrustBundleListByService", mock.Anything, mock.Anything).
+	client.On("TrustBundleListByService", mock.Anything, mock.Anything, mock.Anything).
 		Return(resp, grpcstatus.Error(codes.FailedPrecondition, "peering must be enabled to use this endpoint"))
 
 	// Fetch and assert against the result.
@@ -86,55 +115,3 @@ func TestTrustBundles_badReqType(t *testing.T) {
 	require.Error(t, err)
 	require.Contains(t, err.Error(), "wrong type")
 }
-
-// This test asserts that we can continuously poll this cache type, given that it doesn't support blocking.
-func TestTrustBundles_MultipleUpdates(t *testing.T) {
-	c := cache.New(cache.Options{})
-
-	client := NewMockTrustBundleLister(t)
-
-	// On each mock client call to TrustBundleList by service we will increment the index by 1
-	// to simulate new data arriving.
-	resp := &pbpeering.TrustBundleListByServiceResponse{
-		Index: uint64(0),
-	}
-
-	client.On("TrustBundleListByService", mock.Anything, mock.Anything).
-		Run(func(args mock.Arguments) {
-			req := args.Get(1).(*pbpeering.TrustBundleListByServiceRequest)
-			require.Equal(t, "foo", req.ServiceName)
-
-			// Increment on each call.
-			resp.Index++
-		}).
-		Return(resp, nil)
-
-	c.RegisterType(TrustBundleListName, &TrustBundles{Client: client})
-
-	ch := make(chan cache.UpdateEvent)
-	ctx, cancel := context.WithTimeout(context.Background(), 5*time.Second)
-	t.Cleanup(cancel)
-
-	err := c.Notify(ctx, TrustBundleListName, &TrustBundleListRequest{
-		Request: &pbpeering.TrustBundleListByServiceRequest{ServiceName: "foo"},
-	}, "updates", ch)
-	require.NoError(t, err)
-
-	i := uint64(1)
-	for {
-		select {
-		case <-ctx.Done():
-			t.Fatal("context deadline exceeded")
-			return
-		case update := <-ch:
-			// Expect to receive updates for increasing indexes serially.
-			resp := update.Result.(*pbpeering.TrustBundleListByServiceResponse)
-			require.Equal(t, i, resp.Index)
-			i++
-
-			if i > 3 {
-				return
-			}
-		}
-	}
-}
diff --git a/agent/consul/acl_endpoint.go b/agent/consul/acl_endpoint.go
index cc1632cf4..5d5ba3cb4 100644
--- a/agent/consul/acl_endpoint.go
+++ b/agent/consul/acl_endpoint.go
@@ -1113,7 +1113,7 @@ func (a *ACL) PolicyResolve(args *structs.ACLPolicyBatchGetRequest, reply *struc
 		}
 	}
 
-	a.srv.setQueryMeta(&reply.QueryMeta, args.Token)
+	a.srv.SetQueryMeta(&reply.QueryMeta, args.Token)
 
 	return nil
 }
@@ -1520,7 +1520,7 @@ func (a *ACL) RoleResolve(args *structs.ACLRoleBatchGetRequest, reply *structs.A
 		}
 	}
 
-	a.srv.setQueryMeta(&reply.QueryMeta, args.Token)
+	a.srv.SetQueryMeta(&reply.QueryMeta, args.Token)
 
 	return nil
 }
diff --git a/agent/consul/gateway_locator.go b/agent/consul/gateway_locator.go
index 7ae492822..8f8ca29fb 100644
--- a/agent/consul/gateway_locator.go
+++ b/agent/consul/gateway_locator.go
@@ -14,6 +14,7 @@ import (
 	"github.com/hashicorp/go-hclog"
 	memdb "github.com/hashicorp/go-memdb"
 
+	"github.com/hashicorp/consul/agent/blockingquery"
 	"github.com/hashicorp/consul/agent/consul/state"
 	"github.com/hashicorp/consul/agent/structs"
 	"github.com/hashicorp/consul/api"
@@ -273,7 +274,7 @@ func getRandomItem(items []string) string {
 }
 
 type serverDelegate interface {
-	blockingQuery(queryOpts blockingQueryOptions, queryMeta blockingQueryResponseMeta, fn queryFn) error
+	blockingQuery(requestOpts blockingquery.RequestOptions, responseMeta blockingquery.ResponseMeta, query blockingquery.QueryFn) error
 	IsLeader() bool
 	LeaderLastContact() time.Time
 	setDatacenterSupportsFederationStates()
diff --git a/agent/consul/gateway_locator_test.go b/agent/consul/gateway_locator_test.go
index ddd48e0b1..f9b1daf26 100644
--- a/agent/consul/gateway_locator_test.go
+++ b/agent/consul/gateway_locator_test.go
@@ -13,6 +13,7 @@ import (
 	"github.com/stretchr/testify/assert"
 	"github.com/stretchr/testify/require"
 
+	"github.com/hashicorp/consul/agent/blockingquery"
 	"github.com/hashicorp/consul/agent/consul/state"
 	"github.com/hashicorp/consul/agent/structs"
 	"github.com/hashicorp/consul/api"
@@ -475,6 +476,8 @@ func TestGatewayLocator(t *testing.T) {
 	})
 }
 
+var _ serverDelegate = (*testServerDelegate)(nil)
+
 type testServerDelegate struct {
 	dcSupportsFederationStates int32 // atomically accessed, at start to prevent alignment issues
 
@@ -496,9 +499,9 @@ func (d *testServerDelegate) datacenterSupportsFederationStates() bool {
 
 // This is just enough to exercise the logic.
 func (d *testServerDelegate) blockingQuery(
-	queryOpts blockingQueryOptions,
-	queryMeta blockingQueryResponseMeta,
-	fn queryFn,
+	queryOpts blockingquery.RequestOptions,
+	queryMeta blockingquery.ResponseMeta,
+	fn blockingquery.QueryFn,
 ) error {
 	minQueryIndex := queryOpts.GetMinQueryIndex()
 
diff --git a/agent/consul/internal_endpoint.go b/agent/consul/internal_endpoint.go
index bfe12864d..16dab8c22 100644
--- a/agent/consul/internal_endpoint.go
+++ b/agent/consul/internal_endpoint.go
@@ -815,7 +815,7 @@ func (m *Internal) EventFire(args *structs.EventFireRequest,
 	}
 
 	// Set the query meta data
-	m.srv.setQueryMeta(&reply.QueryMeta, args.Token)
+	m.srv.SetQueryMeta(&reply.QueryMeta, args.Token)
 
 	// Add the consul prefix to the event name
 	eventName := userEventName(args.Name)
diff --git a/agent/consul/prepared_query_endpoint.go b/agent/consul/prepared_query_endpoint.go
index df4ffdc1c..101839708 100644
--- a/agent/consul/prepared_query_endpoint.go
+++ b/agent/consul/prepared_query_endpoint.go
@@ -312,9 +312,9 @@ func (p *PreparedQuery) Explain(args *structs.PreparedQueryExecuteRequest,
 	defer metrics.MeasureSince([]string{"prepared-query", "explain"}, time.Now())
 
 	// We have to do this ourselves since we are not doing a blocking RPC.
-	p.srv.setQueryMeta(&reply.QueryMeta, args.Token)
+	p.srv.SetQueryMeta(&reply.QueryMeta, args.Token)
 	if args.RequireConsistent {
-		if err := p.srv.consistentRead(); err != nil {
+		if err := p.srv.ConsistentRead(); err != nil {
 			return err
 		}
 	}
@@ -360,7 +360,7 @@ func (p *PreparedQuery) Execute(args *structs.PreparedQueryExecuteRequest,
 
 	// We have to do this ourselves since we are not doing a blocking RPC.
 	if args.RequireConsistent {
-		if err := p.srv.consistentRead(); err != nil {
+		if err := p.srv.ConsistentRead(); err != nil {
 			return err
 		}
 	}
@@ -404,7 +404,7 @@ func (p *PreparedQuery) Execute(args *structs.PreparedQueryExecuteRequest,
 		// though, since this is essentially a misconfiguration.
 
 		// We have to do this ourselves since we are not doing a blocking RPC.
-		p.srv.setQueryMeta(&reply.QueryMeta, token)
+		p.srv.SetQueryMeta(&reply.QueryMeta, token)
 
 		// Shuffle the results in case coordinates are not available if they
 		// requested an RTT sort.
@@ -506,7 +506,7 @@ func (p *PreparedQuery) ExecuteRemote(args *structs.PreparedQueryExecuteRemoteRe
 
 	// We have to do this ourselves since we are not doing a blocking RPC.
 	if args.RequireConsistent {
-		if err := p.srv.consistentRead(); err != nil {
+		if err := p.srv.ConsistentRead(); err != nil {
 			return err
 		}
 	}
@@ -527,7 +527,7 @@ func (p *PreparedQuery) ExecuteRemote(args *structs.PreparedQueryExecuteRemoteRe
 	}
 
 	// We have to do this ourselves since we are not doing a blocking RPC.
-	p.srv.setQueryMeta(&reply.QueryMeta, token)
+	p.srv.SetQueryMeta(&reply.QueryMeta, token)
 
 	// We don't bother trying to do an RTT sort here since we are by
 	// definition in another DC. We just shuffle to make sure that we
diff --git a/agent/consul/rpc.go b/agent/consul/rpc.go
index 1d87774fd..f97a5ff88 100644
--- a/agent/consul/rpc.go
+++ b/agent/consul/rpc.go
@@ -13,7 +13,6 @@ import (
 	"math"
 	"net"
 	"strings"
-	"sync/atomic"
 	"time"
 
 	"github.com/armon/go-metrics"
@@ -30,6 +29,7 @@ import (
 	msgpackrpc "github.com/hashicorp/consul-net-rpc/net-rpc-msgpackrpc"
 
 	"github.com/hashicorp/consul/acl"
+	"github.com/hashicorp/consul/agent/blockingquery"
 	"github.com/hashicorp/consul/agent/consul/rate"
 	"github.com/hashicorp/consul/agent/consul/state"
 	"github.com/hashicorp/consul/agent/consul/wanfed"
@@ -1018,167 +1018,26 @@ type blockingQueryResponseMeta interface {
 	SetResultsFilteredByACLs(bool)
 }
 
-// blockingQuery performs a blocking query if opts.GetMinQueryIndex is
-// greater than 0, otherwise performs a non-blocking query. Blocking queries will
-// block until responseMeta.Index is greater than opts.GetMinQueryIndex,
-// or opts.GetMaxQueryTime is reached. Non-blocking queries return immediately
-// after performing the query.
-//
-// If opts.GetRequireConsistent is true, blockingQuery will first verify it is
-// still the cluster leader before performing the query.
-//
-// The query function is expected to be a closure that has access to responseMeta
-// so that it can set the Index. The actual result of the query is opaque to blockingQuery.
-//
-// The query function can return errNotFound, which is a sentinel error. Returning
-// errNotFound indicates that the query found no results, which allows
-// blockingQuery to keep blocking until the query returns a non-nil error.
-// The query function must take care to set the actual result of the query to
-// nil in these cases, otherwise when blockingQuery times out it may return
-// a previous result. errNotFound will never be returned to the caller, it is
-// converted to nil before returning.
-//
-// The query function can return errNotChanged, which is a sentinel error. This
-// can only be returned on calls AFTER the first call, as it would not be
-// possible to detect the absence of a change on the first call. Returning
-// errNotChanged indicates that the query results are identical to the prior
-// results which allows blockingQuery to keep blocking until the query returns
-// a real changed result.
-//
-// The query function must take care to ensure the actual result of the query
-// is either left unmodified or explicitly left in a good state before
-// returning, otherwise when blockingQuery times out it may return an
-// incomplete or unexpected result. errNotChanged will never be returned to the
-// caller, it is converted to nil before returning.
-//
-// If query function returns any other error, the error is returned to the caller
-// immediately.
-//
-// The query function must follow these rules:
-//
-//  1. to access data it must use the passed in state.Store.
-//  2. it must set the responseMeta.Index to an index greater than
-//     opts.GetMinQueryIndex if the results return by the query have changed.
-//  3. any channels added to the memdb.WatchSet must unblock when the results
-//     returned by the query have changed.
-//
-// To ensure optimal performance of the query, the query function should make a
-// best-effort attempt to follow these guidelines:
-//
-//  1. only set responseMeta.Index to an index greater than
-//     opts.GetMinQueryIndex when the results returned by the query have changed.
-//  2. any channels added to the memdb.WatchSet should only unblock when the
-//     results returned by the query have changed.
+// blockingQuery is a passthrough to blockingquery.Query that keeps API
+// compatibility with Server. That has RPC and FSM machinery mixed in the same consul
+// package.
 func (s *Server) blockingQuery(
-	opts blockingQueryOptions,
-	responseMeta blockingQueryResponseMeta,
-	query queryFn,
+	requestOpts blockingquery.RequestOptions,
+	responseMeta blockingquery.ResponseMeta,
+	query blockingquery.QueryFn,
 ) error {
-	var ctx context.Context = &lib.StopChannelContext{StopCh: s.shutdownCh}
-
-	metrics.IncrCounter([]string{"rpc", "query"}, 1)
-
-	minQueryIndex := opts.GetMinQueryIndex()
-	// Perform a non-blocking query
-	if minQueryIndex == 0 {
-		if opts.GetRequireConsistent() {
-			if err := s.consistentRead(); err != nil {
-				return err
-			}
-		}
-
-		var ws memdb.WatchSet
-		err := query(ws, s.fsm.State())
-		s.setQueryMeta(responseMeta, opts.GetToken())
-		if errors.Is(err, errNotFound) || errors.Is(err, errNotChanged) {
-			return nil
-		}
-		return err
-	}
-
-	maxQueryTimeout, err := opts.GetMaxQueryTime()
-	if err != nil {
-		return err
-	}
-	timeout := s.rpcQueryTimeout(maxQueryTimeout)
-	ctx, cancel := context.WithTimeout(ctx, timeout)
-	defer cancel()
-
-	count := atomic.AddUint64(&s.queriesBlocking, 1)
-	metrics.SetGauge([]string{"rpc", "queries_blocking"}, float32(count))
-	// decrement the count when the function returns.
-	defer atomic.AddUint64(&s.queriesBlocking, ^uint64(0))
-
-	var (
-		notFound bool
-		ranOnce  bool
-	)
-
-	for {
-		if opts.GetRequireConsistent() {
-			if err := s.consistentRead(); err != nil {
-				return err
-			}
-		}
-
-		// Operate on a consistent set of state. This makes sure that the
-		// abandon channel goes with the state that the caller is using to
-		// build watches.
-		state := s.fsm.State()
-
-		ws := memdb.NewWatchSet()
-		// This channel will be closed if a snapshot is restored and the
-		// whole state store is abandoned.
-		ws.Add(state.AbandonCh())
-
-		err := query(ws, state)
-		s.setQueryMeta(responseMeta, opts.GetToken())
-
-		switch {
-		case errors.Is(err, errNotFound):
-			if notFound {
-				// query result has not changed
-				minQueryIndex = responseMeta.GetIndex()
-			}
-			notFound = true
-		case errors.Is(err, errNotChanged):
-			if ranOnce {
-				// query result has not changed
-				minQueryIndex = responseMeta.GetIndex()
-			}
-		case err != nil:
-			return err
-		}
-		ranOnce = true
-
-		if responseMeta.GetIndex() > minQueryIndex {
-			return nil
-		}
-
-		// block until something changes, or the timeout
-		if err := ws.WatchCtx(ctx); err != nil {
-			// exit if we've reached the timeout, or other cancellation
-			return nil
-		}
-
-		// exit if the state store has been abandoned
-		select {
-		case <-state.AbandonCh():
-			return nil
-		default:
-		}
-	}
+	return blockingquery.Query(s, requestOpts, responseMeta, query)
 }
 
 var (
-	errNotFound   = fmt.Errorf("no data found for query")
-	errNotChanged = fmt.Errorf("data did not change for query")
+	errNotFound   = blockingquery.ErrNotFound
+	errNotChanged = blockingquery.ErrNotChanged
 )
 
-// setQueryMeta is used to populate the QueryMeta data for an RPC call
+// SetQueryMeta is used to populate the QueryMeta data for an RPC call
 //
 // Note: This method must be called *after* filtering query results with ACLs.
-func (s *Server) setQueryMeta(m blockingQueryResponseMeta, token string) {
+func (s *Server) SetQueryMeta(m blockingquery.ResponseMeta, token string) {
 	if s.IsLeader() {
 		m.SetLastContact(0)
 		m.SetKnownLeader(true)
@@ -1240,19 +1099,19 @@ func (s *Server) consistentReadWithContext(ctx context.Context) error {
 	}
 }
 
-// consistentRead is used to ensure we do not perform a stale
+// ConsistentRead is used to ensure we do not perform a stale
 // read. This is done by verifying leadership before the read.
-func (s *Server) consistentRead() error {
+func (s *Server) ConsistentRead() error {
 	ctx, cancel := context.WithTimeout(context.Background(), s.config.RPCHoldTimeout)
 	defer cancel()
 
 	return s.consistentReadWithContext(ctx)
 }
 
-// rpcQueryTimeout calculates the timeout for the query, ensures it is
+// RPCQueryTimeout calculates the timeout for the query, ensures it is
 // constrained to the configured limit, and adds jitter to prevent multiple
 // blocking queries from all timing out at the same time.
-func (s *Server) rpcQueryTimeout(queryTimeout time.Duration) time.Duration {
+func (s *Server) RPCQueryTimeout(queryTimeout time.Duration) time.Duration {
 	// Restrict the max query time, and ensure there is always one.
 	if queryTimeout > s.config.MaxQueryTime {
 		queryTimeout = s.config.MaxQueryTime
diff --git a/agent/consul/rpc_test.go b/agent/consul/rpc_test.go
index a4b7f7faa..f1b05fa52 100644
--- a/agent/consul/rpc_test.go
+++ b/agent/consul/rpc_test.go
@@ -502,7 +502,7 @@ func TestRPC_ReadyForConsistentReads(t *testing.T) {
 	}
 
 	s.resetConsistentReadReady()
-	err := s.consistentRead()
+	err := s.ConsistentRead()
 	if err.Error() != "Not ready to serve consistent reads" {
 		t.Fatal("Server should NOT be ready for consistent reads")
 	}
@@ -513,7 +513,7 @@ func TestRPC_ReadyForConsistentReads(t *testing.T) {
 	}()
 
 	retry.Run(t, func(r *retry.R) {
-		if err := s.consistentRead(); err != nil {
+		if err := s.ConsistentRead(); err != nil {
 			r.Fatalf("Expected server to be ready for consistent reads, got error %v", err)
 		}
 	})
diff --git a/agent/consul/server.go b/agent/consul/server.go
index 294417c5e..6c6afc015 100644
--- a/agent/consul/server.go
+++ b/agent/consul/server.go
@@ -39,6 +39,7 @@ import (
 
 	"github.com/hashicorp/consul/acl"
 	"github.com/hashicorp/consul/acl/resolver"
+	"github.com/hashicorp/consul/agent/blockingquery"
 	"github.com/hashicorp/consul/agent/consul/authmethod"
 	"github.com/hashicorp/consul/agent/consul/authmethod/ssoauth"
 	"github.com/hashicorp/consul/agent/consul/fsm"
@@ -173,6 +174,8 @@ type raftStore interface {
 
 const requestLimitsBurstMultiplier = 10
 
+var _ blockingquery.FSMServer = (*Server)(nil)
+
 // Server is Consul server which manages the service discovery,
 // health checking, DC forwarding, Raft, and multiple Serf pools.
 type Server struct {
@@ -447,6 +450,18 @@ type Server struct {
 	reportingManager *reporting.ReportingManager
 }
 
+func (s *Server) DecrementBlockingQueries() uint64 {
+	return atomic.AddUint64(&s.queriesBlocking, ^uint64(0))
+}
+
+func (s *Server) GetShutdownChannel() chan struct{} {
+	return s.shutdownCh
+}
+
+func (s *Server) IncrementBlockingQueries() uint64 {
+	return atomic.AddUint64(&s.queriesBlocking, 1)
+}
+
 type connHandler interface {
 	Run() error
 	Handle(conn net.Conn)
@@ -875,6 +890,7 @@ func newGRPCHandlerFromConfig(deps Deps, config *Config, s *Server) connHandler
 		ConnectEnabled: config.ConnectEnabled,
 		PeeringEnabled: config.PeeringEnabled,
 		Locality:       config.Locality,
+		FSMServer:      s,
 	})
 	s.peeringServer = p
 	o := operator.NewServer(operator.Config{
@@ -1819,6 +1835,13 @@ func (s *Server) FSM() *fsm.FSM {
 	return s.fsm
 }
 
+func (s *Server) GetState() *state.Store {
+	if s == nil || s.FSM() == nil {
+		return nil
+	}
+	return s.FSM().State()
+}
+
 // Stats is used to return statistics for debugging and insight
 // for various sub-systems
 func (s *Server) Stats() map[string]map[string]string {
diff --git a/agent/consul/snapshot_endpoint.go b/agent/consul/snapshot_endpoint.go
index 4c77a3efb..7e5f21113 100644
--- a/agent/consul/snapshot_endpoint.go
+++ b/agent/consul/snapshot_endpoint.go
@@ -71,14 +71,14 @@ func (s *Server) dispatchSnapshotRequest(args *structs.SnapshotRequest, in io.Re
 	switch args.Op {
 	case structs.SnapshotSave:
 		if !args.AllowStale {
-			if err := s.consistentRead(); err != nil {
+			if err := s.ConsistentRead(); err != nil {
 				return nil, err
 			}
 		}
 
 		// Set the metadata here before we do anything; this should always be
 		// pessimistic if we get more data while the snapshot is being taken.
-		s.setQueryMeta(&reply.QueryMeta, args.Token)
+		s.SetQueryMeta(&reply.QueryMeta, args.Token)
 
 		// Take the snapshot and capture the index.
 		snap, err := snapshot.New(s.logger, s.raft)
diff --git a/agent/consul/txn_endpoint.go b/agent/consul/txn_endpoint.go
index df0a70117..e7e5d8708 100644
--- a/agent/consul/txn_endpoint.go
+++ b/agent/consul/txn_endpoint.go
@@ -188,7 +188,7 @@ func (t *Txn) Read(args *structs.TxnReadRequest, reply *structs.TxnReadResponse)
 
 	// We have to do this ourselves since we are not doing a blocking RPC.
 	if args.RequireConsistent {
-		if err := t.srv.consistentRead(); err != nil {
+		if err := t.srv.ConsistentRead(); err != nil {
 			return err
 		}
 	}
@@ -220,7 +220,7 @@ func (t *Txn) Read(args *structs.TxnReadRequest, reply *structs.TxnReadResponse)
 	reply.QueryMeta.ResultsFilteredByACLs = total != len(reply.Results)
 
 	// We have to do this ourselves since we are not doing a blocking RPC.
-	t.srv.setQueryMeta(&reply.QueryMeta, args.Token)
+	t.srv.SetQueryMeta(&reply.QueryMeta, args.Token)
 
 	return nil
 }
diff --git a/agent/grpc-external/metadata_test.go b/agent/grpc-external/options_test.go
similarity index 100%
rename from agent/grpc-external/metadata_test.go
rename to agent/grpc-external/options_test.go
diff --git a/agent/grpc-external/querymeta.go b/agent/grpc-external/querymeta.go
new file mode 100644
index 000000000..55b960255
--- /dev/null
+++ b/agent/grpc-external/querymeta.go
@@ -0,0 +1,77 @@
+package external
+
+import (
+	"fmt"
+	"reflect"
+
+	"github.com/mitchellh/mapstructure"
+	"google.golang.org/grpc/metadata"
+
+	"github.com/hashicorp/consul/agent/structs"
+)
+
+func StringToQueryBackendDecodeHookFunc(f reflect.Type, t reflect.Type, data any) (any, error) {
+	if f.Kind() != reflect.String {
+		return data, nil
+	}
+	if t != reflect.TypeOf(structs.QueryBackend(0)) {
+		return data, nil
+	}
+
+	name, ok := data.(string)
+	if !ok {
+		return data, fmt.Errorf("could not parse query backend as string")
+	}
+
+	return structs.QueryBackendFromString(name), nil
+}
+
+// QueryMetaFromGRPCMeta returns a structs.QueryMeta struct parsed from the metadata.MD,
+// such as from a gRPC header or trailer.
+func QueryMetaFromGRPCMeta(md metadata.MD) (structs.QueryMeta, error) {
+	var queryMeta structs.QueryMeta
+
+	m := map[string]string{}
+	for k, v := range md {
+		m[k] = v[0]
+	}
+
+	decodeHooks := mapstructure.ComposeDecodeHookFunc(
+		mapstructure.StringToTimeDurationHookFunc(),
+		StringToQueryBackendDecodeHookFunc,
+	)
+
+	config := &mapstructure.DecoderConfig{
+		Metadata:         nil,
+		Result:           &queryMeta,
+		WeaklyTypedInput: true,
+		DecodeHook:       decodeHooks,
+	}
+
+	decoder, err := mapstructure.NewDecoder(config)
+	if err != nil {
+		return queryMeta, err
+	}
+
+	err = decoder.Decode(m)
+	if err != nil {
+		return queryMeta, err
+	}
+
+	return queryMeta, nil
+}
+
+// GRPCMetadataFromQueryMeta returns a metadata struct with fields from the structs.QueryMeta attached.
+// The return value is suitable for attaching to a gRPC header/trailer.
+func GRPCMetadataFromQueryMeta(queryMeta structs.QueryMeta) (metadata.MD, error) {
+	md := metadata.MD{}
+	m := map[string]any{}
+	err := mapstructure.Decode(queryMeta, &m)
+	if err != nil {
+		return nil, err
+	}
+	for k, v := range m {
+		md.Set(k, fmt.Sprintf("%v", v))
+	}
+	return md, nil
+}
diff --git a/agent/grpc-external/querymeta_test.go b/agent/grpc-external/querymeta_test.go
new file mode 100644
index 000000000..66c7136a3
--- /dev/null
+++ b/agent/grpc-external/querymeta_test.go
@@ -0,0 +1,35 @@
+package external
+
+import (
+	"testing"
+	"time"
+
+	"github.com/stretchr/testify/require"
+
+	"github.com/hashicorp/consul/agent/structs"
+)
+
+func TestQueryMetaFromGRPCMetaRoundTrip(t *testing.T) {
+	lastContact, err := time.ParseDuration("1s")
+	require.NoError(t, err)
+
+	expected := structs.QueryMeta{
+		Index:                 42,
+		LastContact:           lastContact,
+		KnownLeader:           true,
+		ConsistencyLevel:      "stale",
+		NotModified:           true,
+		Backend:               structs.QueryBackend(0),
+		ResultsFilteredByACLs: true,
+	}
+
+	md, err := GRPCMetadataFromQueryMeta(expected)
+	require.NoError(t, err)
+
+	actual, err := QueryMetaFromGRPCMeta(md)
+	if err != nil {
+		t.Fatal(err)
+	}
+
+	require.Equal(t, expected, actual)
+}
diff --git a/agent/peering_endpoint.go b/agent/peering_endpoint.go
index 5047958c7..8372c94c2 100644
--- a/agent/peering_endpoint.go
+++ b/agent/peering_endpoint.go
@@ -8,6 +8,9 @@ import (
 	"net/http"
 	"strings"
 
+	"google.golang.org/grpc"
+	"google.golang.org/grpc/metadata"
+
 	"github.com/hashicorp/consul/acl"
 	external "github.com/hashicorp/consul/agent/grpc-external"
 	"github.com/hashicorp/consul/agent/structs"
@@ -49,12 +52,14 @@ func (s *HTTPHandlers) peeringRead(resp http.ResponseWriter, req *http.Request,
 	var dc string
 	options := structs.QueryOptions{}
 	s.parse(resp, req, &dc, &options)
+	options.AllowStale = false // To get all information on a peering, this request must be forward to a leader
 	ctx, err := external.ContextWithQueryOptions(req.Context(), options)
 	if err != nil {
 		return nil, err
 	}
 
-	result, err := s.agent.rpcClientPeering.PeeringRead(ctx, &args)
+	var header metadata.MD
+	result, err := s.agent.rpcClientPeering.PeeringRead(ctx, &args, grpc.Header(&header))
 	if err != nil {
 		return nil, err
 	}
@@ -62,6 +67,14 @@ func (s *HTTPHandlers) peeringRead(resp http.ResponseWriter, req *http.Request,
 		return nil, HTTPError{StatusCode: http.StatusNotFound, Reason: fmt.Sprintf("Peering not found for %q", name)}
 	}
 
+	meta, err := external.QueryMetaFromGRPCMeta(header)
+	if err != nil {
+		return result.Peering.ToAPI(), fmt.Errorf("could not convert gRPC metadata to query meta: %w", err)
+	}
+	if err := setMeta(resp, &meta); err != nil {
+		return nil, err
+	}
+
 	return result.Peering.ToAPI(), nil
 }
 
@@ -78,16 +91,26 @@ func (s *HTTPHandlers) PeeringList(resp http.ResponseWriter, req *http.Request)
 	var dc string
 	options := structs.QueryOptions{}
 	s.parse(resp, req, &dc, &options)
+	options.AllowStale = false // To get all information on a peering, this request must be forward to a leader
 	ctx, err := external.ContextWithQueryOptions(req.Context(), options)
 	if err != nil {
 		return nil, err
 	}
 
-	pbresp, err := s.agent.rpcClientPeering.PeeringList(ctx, &args)
+	var header metadata.MD
+	pbresp, err := s.agent.rpcClientPeering.PeeringList(ctx, &args, grpc.Header(&header))
 	if err != nil {
 		return nil, err
 	}
 
+	meta, err := external.QueryMetaFromGRPCMeta(header)
+	if err != nil {
+		return pbresp.ToAPI(), fmt.Errorf("could not convert gRPC metadata to query meta: %w", err)
+	}
+	if err := setMeta(resp, &meta); err != nil {
+		return nil, err
+	}
+
 	return pbresp.ToAPI(), nil
 }
 
diff --git a/agent/peering_endpoint_test.go b/agent/peering_endpoint_test.go
index 99d6cb6c3..7ec63c1cd 100644
--- a/agent/peering_endpoint_test.go
+++ b/agent/peering_endpoint_test.go
@@ -563,6 +563,13 @@ func TestHTTP_Peering_Read(t *testing.T) {
 		a.srv.h.ServeHTTP(resp, req)
 		require.Equal(t, http.StatusOK, resp.Code)
 
+		httpResult := resp.Result()
+		_, ok := httpResult.Header["X-Consul-Index"]
+		require.True(t, ok)
+		idx, err := strconv.Atoi(httpResult.Header.Get("X-Consul-Index"))
+		require.NoError(t, err)
+		require.Greater(t, idx, 0) // the raft index is not deterministic at this point
+
 		var apiResp api.Peering
 		require.NoError(t, json.NewDecoder(resp.Body).Decode(&apiResp))
 
@@ -692,6 +699,13 @@ func TestHTTP_Peering_List(t *testing.T) {
 		a.srv.h.ServeHTTP(resp, req)
 		require.Equal(t, http.StatusOK, resp.Code)
 
+		httpResult := resp.Result()
+		_, ok := httpResult.Header["X-Consul-Index"]
+		require.True(t, ok)
+		idx, err := strconv.Atoi(httpResult.Header.Get("X-Consul-Index"))
+		require.NoError(t, err)
+		require.Greater(t, idx, 0) // the raft index is not deterministic at this point
+
 		var apiResp []*api.Peering
 		require.NoError(t, json.NewDecoder(resp.Body).Decode(&apiResp))
 
diff --git a/agent/proxycfg-glue/peering_list.go b/agent/proxycfg-glue/peering_list.go
index c783f0219..219bf9b95 100644
--- a/agent/proxycfg-glue/peering_list.go
+++ b/agent/proxycfg-glue/peering_list.go
@@ -52,8 +52,8 @@ func (s *serverPeeringList) Notify(ctx context.Context, req *cachetype.PeeringLi
 				return 0, nil, err
 			}
 			return index, &pbpeering.PeeringListResponse{
-				Index:    index,
-				Peerings: peerings,
+				OBSOLETE_Index: index,
+				Peerings:       peerings,
 			}, nil
 		},
 		dispatchBlockingQueryUpdate[*pbpeering.PeeringListResponse](ch),
diff --git a/agent/proxycfg-glue/peering_list_test.go b/agent/proxycfg-glue/peering_list_test.go
index ad196cccd..f570dbbcc 100644
--- a/agent/proxycfg-glue/peering_list_test.go
+++ b/agent/proxycfg-glue/peering_list_test.go
@@ -48,7 +48,7 @@ func TestServerPeeringList(t *testing.T) {
 		result := getEventResult[*pbpeering.PeeringListResponse](t, eventCh)
 		require.Len(t, result.Peerings, 1)
 		require.Equal(t, "peer-01", result.Peerings[0].Name)
-		require.Equal(t, index, result.Index)
+		require.Equal(t, index, result.OBSOLETE_Index)
 	})
 
 	testutil.RunStep(t, "add peering", func(t *testing.T) {
@@ -63,7 +63,7 @@ func TestServerPeeringList(t *testing.T) {
 		result := getEventResult[*pbpeering.PeeringListResponse](t, eventCh)
 		require.Len(t, result.Peerings, 2)
 		require.Equal(t, "peer-02", result.Peerings[1].Name)
-		require.Equal(t, index+1, result.Index)
+		require.Equal(t, index+1, result.OBSOLETE_Index)
 	})
 }
 
@@ -100,7 +100,7 @@ func TestServerPeeringList_ACLEnforcement(t *testing.T) {
 		result := getEventResult[*pbpeering.PeeringListResponse](t, eventCh)
 		require.Len(t, result.Peerings, 1)
 		require.Equal(t, "peer-01", result.Peerings[0].Name)
-		require.Equal(t, index, result.Index)
+		require.Equal(t, index, result.OBSOLETE_Index)
 	})
 
 	testutil.RunStep(t, "can't read", func(t *testing.T) {
diff --git a/agent/proxycfg-glue/trust_bundle.go b/agent/proxycfg-glue/trust_bundle.go
index 7e2ad127f..108e7ea9f 100644
--- a/agent/proxycfg-glue/trust_bundle.go
+++ b/agent/proxycfg-glue/trust_bundle.go
@@ -59,8 +59,8 @@ func (s *serverTrustBundle) Notify(ctx context.Context, req *cachetype.TrustBund
 				return 0, nil, err
 			}
 			return index, &pbpeering.TrustBundleReadResponse{
-				Index:  index,
-				Bundle: bundle,
+				OBSOLETE_Index: index,
+				Bundle:         bundle,
 			}, nil
 		},
 		dispatchBlockingQueryUpdate[*pbpeering.TrustBundleReadResponse](ch),
@@ -116,8 +116,8 @@ func (s *serverTrustBundleList) Notify(ctx context.Context, req *cachetype.Trust
 			}
 
 			return index, &pbpeering.TrustBundleListByServiceResponse{
-				Index:   index,
-				Bundles: bundles,
+				OBSOLETE_Index: index,
+				Bundles:        bundles,
 			}, nil
 		},
 		dispatchBlockingQueryUpdate[*pbpeering.TrustBundleListByServiceResponse](ch),
diff --git a/agent/proxycfg/mesh_gateway.go b/agent/proxycfg/mesh_gateway.go
index c423644b3..2267a2960 100644
--- a/agent/proxycfg/mesh_gateway.go
+++ b/agent/proxycfg/mesh_gateway.go
@@ -12,9 +12,10 @@ import (
 	"strings"
 	"time"
 
-	"github.com/hashicorp/consul/acl"
 	"github.com/hashicorp/go-hclog"
 
+	"github.com/hashicorp/consul/acl"
+
 	cachetype "github.com/hashicorp/consul/agent/cache-types"
 	"github.com/hashicorp/consul/agent/proxycfg/internal/watch"
 	"github.com/hashicorp/consul/agent/structs"
@@ -615,9 +616,11 @@ func (s *handlerMeshGateway) handleUpdate(ctx context.Context, u UpdateEvent, sn
 
 		peerServers := make(map[string]PeerServersValue)
 		for _, peering := range resp.Peerings {
-			// We only need to keep track of outbound establish connections
-			// for mesh gateway.
-			if !peering.ShouldDial() || !peering.IsActive() {
+			// We only need to keep track of outbound establish connections for mesh gateway.
+			// We could also check for the peering status, but this requires a response from the leader
+			// which holds the peerstream information. We want to allow stale reads so there could be peerings in
+			// a deleting or terminating state.
+			if !peering.ShouldDial() {
 				continue
 			}
 
diff --git a/agent/proxycfg/testing_mesh_gateway.go b/agent/proxycfg/testing_mesh_gateway.go
index f37189251..0ad9d4524 100644
--- a/agent/proxycfg/testing_mesh_gateway.go
+++ b/agent/proxycfg/testing_mesh_gateway.go
@@ -806,14 +806,13 @@ func TestConfigSnapshotPeeredMeshGateway(t testing.T, variant string, nsFn func(
 				CorrelationID: peerServersWatchID,
 				Result: &pbpeering.PeeringListResponse{
 					Peerings: []*pbpeering.Peering{
-						// Not active
+						// Empty state should be included. This could result from a query being served by a follower.
 						{
 							Name:           "peer-a",
 							PeerServerName: connect.PeeringServerSAN("dc2", "f3f41279-001d-42bb-912e-f6103fb036b8"),
 							PeerServerAddresses: []string{
 								"1.2.3.4:5200",
 							},
-							State:       pbpeering.PeeringState_TERMINATED,
 							ModifyIndex: 2,
 						},
 						// No server addresses, so this should only be accepting connections
diff --git a/agent/rpc/peering/service.go b/agent/rpc/peering/service.go
index fe68b3616..f8e89cabb 100644
--- a/agent/rpc/peering/service.go
+++ b/agent/rpc/peering/service.go
@@ -21,16 +21,16 @@ import (
 	"google.golang.org/protobuf/proto"
 	"google.golang.org/protobuf/types/known/timestamppb"
 
-	"github.com/hashicorp/consul/lib/retry"
-
 	"github.com/hashicorp/consul/acl"
 	"github.com/hashicorp/consul/acl/resolver"
+	"github.com/hashicorp/consul/agent/blockingquery"
 	"github.com/hashicorp/consul/agent/consul/state"
 	"github.com/hashicorp/consul/agent/consul/stream"
 	external "github.com/hashicorp/consul/agent/grpc-external"
 	"github.com/hashicorp/consul/agent/grpc-external/services/peerstream"
 	"github.com/hashicorp/consul/agent/structs"
 	"github.com/hashicorp/consul/lib"
+	"github.com/hashicorp/consul/lib/retry"
 	"github.com/hashicorp/consul/proto/private/pbcommon"
 	"github.com/hashicorp/consul/proto/private/pbpeering"
 	"github.com/hashicorp/consul/proto/private/pbpeerstream"
@@ -72,11 +72,13 @@ var writeRequest struct {
 	structs.DCSpecificRequest
 }
 
-var readRequest struct {
+type readRequest struct {
 	structs.QueryOptions
 	structs.DCSpecificRequest
 }
 
+var emptyDCSpecificRequest structs.DCSpecificRequest
+
 // Server implements pbpeering.PeeringService to provide RPC operations for
 // managing peering relationships.
 type Server struct {
@@ -92,6 +94,9 @@ type Config struct {
 	ConnectEnabled bool
 	PeeringEnabled bool
 	Locality       *structs.Locality
+
+	// Needed because the stateful components needed to handle blocking queries are mixed in with server goo
+	FSMServer blockingquery.FSMServer
 }
 
 func NewServer(cfg Config) *Server {
@@ -99,6 +104,7 @@ func NewServer(cfg Config) *Server {
 	requireNotNil(cfg.Tracker, "Tracker")
 	requireNotNil(cfg.Logger, "Logger")
 	requireNotNil(cfg.ForwardRPC, "ForwardRPC")
+	requireNotNil(cfg.FSMServer, "FSMServer")
 	if cfg.Datacenter == "" {
 		panic("Datacenter is required")
 	}
@@ -595,7 +601,10 @@ func retryExchange(ctx context.Context, req *pbpeerstream.ExchangeSecretRequest,
 	return resp, dialErrors
 }
 
-// OPTIMIZE: Handle blocking queries
+// PeeringRead returns the peering of the requested name and partition (enterprise only).
+// Note that for the purposes of the blocking query, changes are only observed as part of the
+// storage Index, which does not include the hydrated state from reconcilePeering, including
+// the Active state and the count of imported/exported services.
 func (s *Server) PeeringRead(ctx context.Context, req *pbpeering.PeeringReadRequest) (*pbpeering.PeeringReadResponse, error) {
 	if !s.Config.PeeringEnabled {
 		return nil, peeringNotEnabledErr
@@ -605,8 +614,13 @@ func (s *Server) PeeringRead(ctx context.Context, req *pbpeering.PeeringReadRequ
 		return nil, grpcstatus.Error(codes.InvalidArgument, err.Error())
 	}
 
+	options, err := external.QueryOptionsFromContext(ctx)
+	if err != nil {
+		return nil, err
+	}
+
 	var resp *pbpeering.PeeringReadResponse
-	handled, err := s.ForwardRPC(&readRequest, func(conn *grpc.ClientConn) error {
+	handled, err := s.ForwardRPC(&readRequest{options, emptyDCSpecificRequest}, func(conn *grpc.ClientConn) error {
 		ctx := external.ForwardMetadataContext(ctx)
 		var err error
 		resp, err = pbpeering.NewPeeringServiceClient(conn).PeeringRead(ctx, req)
@@ -620,10 +634,7 @@ func (s *Server) PeeringRead(ctx context.Context, req *pbpeering.PeeringReadRequ
 
 	var authzCtx acl.AuthorizerContext
 	entMeta := structs.DefaultEnterpriseMetaInPartition(req.Partition)
-	options, err := external.QueryOptionsFromContext(ctx)
-	if err != nil {
-		return nil, err
-	}
+
 	authz, err := s.Backend.ResolveTokenAndDefaultMeta(options.Token, entMeta, &authzCtx)
 	if err != nil {
 		return nil, err
@@ -633,23 +644,45 @@ func (s *Server) PeeringRead(ctx context.Context, req *pbpeering.PeeringReadRequ
 		return nil, err
 	}
 
-	q := state.Query{
-		Value:          strings.ToLower(req.Name),
-		EnterpriseMeta: *entMeta,
-	}
-	_, peering, err := s.Backend.Store().PeeringRead(nil, q)
+	res := &pbpeering.PeeringReadResponse{}
+	meta := structs.QueryMeta{}
+	err = blockingquery.Query(s.FSMServer, &options, &meta, func(ws memdb.WatchSet, store *state.Store) error {
+		q := state.Query{
+			Value:          strings.ToLower(req.Name),
+			EnterpriseMeta: *entMeta,
+		}
+		idx, peering, err := store.PeeringRead(ws, q)
+		if err != nil {
+			return err
+		}
+
+		meta.SetIndex(idx)
+		if peering == nil {
+			return blockingquery.ErrNotFound
+		}
+
+		res.Peering = s.reconcilePeering(peering)
+		return nil
+	})
 	if err != nil {
-		return nil, err
-	}
-	if peering == nil {
-		return &pbpeering.PeeringReadResponse{Peering: nil}, nil
+		return nil, fmt.Errorf("error executing peering read blocking query: %w", err)
 	}
 
-	cp := s.reconcilePeering(peering)
-	return &pbpeering.PeeringReadResponse{Peering: cp}, nil
+	header, err := external.GRPCMetadataFromQueryMeta(meta)
+	if err != nil {
+		return nil, fmt.Errorf("could not convert query metadata to gRPC header")
+	}
+	if err := grpc.SendHeader(ctx, header); err != nil {
+		return nil, fmt.Errorf("could not send gRPC header")
+	}
+
+	return res, nil
 }
 
-// OPTIMIZE: Handle blocking queries
+// PeeringList returns the list of peerings in the requested partition(s) (enterprise only).
+// Note that for the purposes of the blocking query, changes are only observed as part of the
+// storage Index, which does not include the hydrated state from reconcilePeering, including
+// the Active state and the count of imported/exported services.
 func (s *Server) PeeringList(ctx context.Context, req *pbpeering.PeeringListRequest) (*pbpeering.PeeringListResponse, error) {
 	if !s.Config.PeeringEnabled {
 		return nil, peeringNotEnabledErr
@@ -659,8 +692,13 @@ func (s *Server) PeeringList(ctx context.Context, req *pbpeering.PeeringListRequ
 		return nil, grpcstatus.Error(codes.InvalidArgument, err.Error())
 	}
 
+	options, err := external.QueryOptionsFromContext(ctx)
+	if err != nil {
+		return nil, err
+	}
+
 	var resp *pbpeering.PeeringListResponse
-	handled, err := s.ForwardRPC(&readRequest, func(conn *grpc.ClientConn) error {
+	handled, err := s.ForwardRPC(&readRequest{options, emptyDCSpecificRequest}, func(conn *grpc.ClientConn) error {
 		ctx := external.ForwardMetadataContext(ctx)
 		var err error
 		resp, err = pbpeering.NewPeeringServiceClient(conn).PeeringList(ctx, req)
@@ -672,10 +710,6 @@ func (s *Server) PeeringList(ctx context.Context, req *pbpeering.PeeringListRequ
 
 	var authzCtx acl.AuthorizerContext
 	entMeta := structs.DefaultEnterpriseMetaInPartition(req.Partition)
-	options, err := external.QueryOptionsFromContext(ctx)
-	if err != nil {
-		return nil, err
-	}
 
 	authz, err := s.Backend.ResolveTokenAndDefaultMeta(options.Token, entMeta, &authzCtx)
 	if err != nil {
@@ -688,19 +722,40 @@ func (s *Server) PeeringList(ctx context.Context, req *pbpeering.PeeringListRequ
 
 	defer metrics.MeasureSince([]string{"peering", "list"}, time.Now())
 
-	idx, peerings, err := s.Backend.Store().PeeringList(nil, *entMeta)
+	res := &pbpeering.PeeringListResponse{}
+	meta := structs.QueryMeta{}
+	err = blockingquery.Query(s.FSMServer, &options, &meta, func(ws memdb.WatchSet, store *state.Store) error {
+		idx, peerings, err := store.PeeringList(ws, *entMeta)
+		if err != nil {
+			return err
+		}
+
+		// reconcile the actual peering state; need to copy over the ds for peering
+		var cPeerings []*pbpeering.Peering
+		for _, p := range peerings {
+			cp := s.reconcilePeering(p)
+			cPeerings = append(cPeerings, cp)
+		}
+
+		res.Peerings = cPeerings
+		meta.SetIndex(idx)
+		res.OBSOLETE_Index = idx // Compatibility with 1.14 API, deprecate in future release
+
+		return nil
+	})
 	if err != nil {
-		return nil, err
+		return nil, fmt.Errorf("error executing peering list blocking query: %w", err)
 	}
 
-	// reconcile the actual peering state; need to copy over the ds for peering
-	var cPeerings []*pbpeering.Peering
-	for _, p := range peerings {
-		cp := s.reconcilePeering(p)
-		cPeerings = append(cPeerings, cp)
+	header, err := external.GRPCMetadataFromQueryMeta(meta)
+	if err != nil {
+		return nil, fmt.Errorf("could not convert query metadata to gRPC header")
+	}
+	if err := grpc.SendHeader(ctx, header); err != nil {
+		return nil, fmt.Errorf("could not send gRPC header")
 	}
 
-	return &pbpeering.PeeringListResponse{Peerings: cPeerings, Index: idx}, nil
+	return res, nil
 }
 
 // TODO(peering): Get rid of this func when we stop using the stream tracker for imported/ exported services and the peering state
@@ -899,7 +954,6 @@ func (s *Server) PeeringDelete(ctx context.Context, req *pbpeering.PeeringDelete
 	return &pbpeering.PeeringDeleteResponse{}, nil
 }
 
-// OPTIMIZE: Handle blocking queries
 func (s *Server) TrustBundleRead(ctx context.Context, req *pbpeering.TrustBundleReadRequest) (*pbpeering.TrustBundleReadResponse, error) {
 	if !s.Config.PeeringEnabled {
 		return nil, peeringNotEnabledErr
@@ -915,7 +969,7 @@ func (s *Server) TrustBundleRead(ctx context.Context, req *pbpeering.TrustBundle
 	}
 
 	var resp *pbpeering.TrustBundleReadResponse
-	handled, err := s.ForwardRPC(&readRequest, func(conn *grpc.ClientConn) error {
+	handled, err := s.ForwardRPC(&readRequest{options, emptyDCSpecificRequest}, func(conn *grpc.ClientConn) error {
 		ctx := external.ForwardMetadataContext(ctx)
 		var err error
 		resp, err = pbpeering.NewPeeringServiceClient(conn).TrustBundleRead(ctx, req)
@@ -941,22 +995,43 @@ func (s *Server) TrustBundleRead(ctx context.Context, req *pbpeering.TrustBundle
 		return nil, err
 	}
 
-	idx, trustBundle, err := s.Backend.Store().PeeringTrustBundleRead(nil, state.Query{
-		Value:          req.Name,
-		EnterpriseMeta: entMeta,
+	res := &pbpeering.TrustBundleReadResponse{}
+	meta := structs.QueryMeta{}
+	err = blockingquery.Query(s.FSMServer, &options, &meta, func(ws memdb.WatchSet, store *state.Store) error {
+		idx, trustBundle, err := store.PeeringTrustBundleRead(ws, state.Query{
+			Value:          req.Name,
+			EnterpriseMeta: entMeta,
+		})
+		if err != nil {
+			return fmt.Errorf("failed to read trust bundle for peer %s: %w", req.Name, err)
+		}
+
+		meta.SetIndex(idx)
+		if trustBundle == nil {
+			return blockingquery.ErrNotFound
+		}
+
+		res.Bundle = trustBundle
+		res.OBSOLETE_Index = idx // Compatibility with 1.14 API, deprecate in future release
+
+		return nil
 	})
 	if err != nil {
-		return nil, fmt.Errorf("failed to read trust bundle for peer %s: %w", req.Name, err)
+		return nil, fmt.Errorf("error executing trust bundle read blocking query: %w", err)
 	}
 
-	return &pbpeering.TrustBundleReadResponse{
-		Index:  idx,
-		Bundle: trustBundle,
-	}, nil
+	header, err := external.GRPCMetadataFromQueryMeta(meta)
+	if err != nil {
+		return nil, fmt.Errorf("could not convert query metadata to gRPC header")
+	}
+	if err := grpc.SendHeader(ctx, header); err != nil {
+		return nil, fmt.Errorf("could not send gRPC header")
+	}
+
+	return res, nil
 }
 
 // TODO(peering): rename rpc & request/response to drop the "service" part
-// OPTIMIZE: Handle blocking queries
 func (s *Server) TrustBundleListByService(ctx context.Context, req *pbpeering.TrustBundleListByServiceRequest) (*pbpeering.TrustBundleListByServiceResponse, error) {
 	if !s.Config.PeeringEnabled {
 		return nil, peeringNotEnabledErr
@@ -972,8 +1047,13 @@ func (s *Server) TrustBundleListByService(ctx context.Context, req *pbpeering.Tr
 		return nil, errors.New("missing service name")
 	}
 
+	options, err := external.QueryOptionsFromContext(ctx)
+	if err != nil {
+		return nil, err
+	}
+
 	var resp *pbpeering.TrustBundleListByServiceResponse
-	handled, err := s.ForwardRPC(&readRequest, func(conn *grpc.ClientConn) error {
+	handled, err := s.ForwardRPC(&readRequest{options, emptyDCSpecificRequest}, func(conn *grpc.ClientConn) error {
 		ctx := external.ForwardMetadataContext(ctx)
 		var err error
 		resp, err = pbpeering.NewPeeringServiceClient(conn).TrustBundleListByService(ctx, req)
@@ -987,10 +1067,6 @@ func (s *Server) TrustBundleListByService(ctx context.Context, req *pbpeering.Tr
 
 	var authzCtx acl.AuthorizerContext
 	entMeta := acl.NewEnterpriseMetaWithPartition(req.Partition, req.Namespace)
-	options, err := external.QueryOptionsFromContext(ctx)
-	if err != nil {
-		return nil, err
-	}
 
 	authz, err := s.Backend.ResolveTokenAndDefaultMeta(options.Token, &entMeta, &authzCtx)
 	if err != nil {
@@ -1001,26 +1077,47 @@ func (s *Server) TrustBundleListByService(ctx context.Context, req *pbpeering.Tr
 		return nil, err
 	}
 
-	var (
-		idx     uint64
-		bundles []*pbpeering.PeeringTrustBundle
-	)
+	res := &pbpeering.TrustBundleListByServiceResponse{}
+	meta := structs.QueryMeta{}
+	err = blockingquery.Query(s.FSMServer, &options, &meta, func(ws memdb.WatchSet, store *state.Store) error {
+		var (
+			idx     uint64
+			bundles []*pbpeering.PeeringTrustBundle
+		)
+		switch {
+		case req.Kind == string(structs.ServiceKindMeshGateway):
+			idx, bundles, err = store.PeeringTrustBundleList(ws, entMeta)
+		case req.ServiceName != "":
+			idx, bundles, err = store.TrustBundleListByService(ws, req.ServiceName, s.Datacenter, entMeta)
+		case req.Kind != "":
+			return grpcstatus.Error(codes.InvalidArgument, "kind must be mesh-gateway if set")
+		default:
+			return grpcstatus.Error(codes.InvalidArgument, "one of service or kind is required")
+		}
 
-	switch {
-	case req.Kind == string(structs.ServiceKindMeshGateway):
-		idx, bundles, err = s.Backend.Store().PeeringTrustBundleList(nil, entMeta)
-	case req.ServiceName != "":
-		idx, bundles, err = s.Backend.Store().TrustBundleListByService(nil, req.ServiceName, s.Datacenter, entMeta)
-	case req.Kind != "":
-		return nil, grpcstatus.Error(codes.InvalidArgument, "kind must be mesh-gateway if set")
-	default:
-		return nil, grpcstatus.Error(codes.InvalidArgument, "one of service or kind is required")
-	}
+		if err != nil {
+			return fmt.Errorf("error listing trust bundles from store: %w", err)
+		}
 
+		res.Bundles = bundles
+		meta.SetIndex(idx)
+		res.OBSOLETE_Index = idx // Compatibility with 1.14 API, deprecate in future release
+
+		return nil
+	})
 	if err != nil {
-		return nil, err
+		return nil, fmt.Errorf("error executing trust bundle list blocking query: %w", err)
 	}
-	return &pbpeering.TrustBundleListByServiceResponse{Index: idx, Bundles: bundles}, nil
+
+	header, err := external.GRPCMetadataFromQueryMeta(meta)
+	if err != nil {
+		return nil, fmt.Errorf("could not convert query metadata to gRPC header")
+	}
+	if err := grpc.SendHeader(ctx, header); err != nil {
+		return nil, fmt.Errorf("could not send gRPC header")
+	}
+
+	return res, nil
 }
 
 func (s *Server) getExistingPeering(peerName, partition string) (*pbpeering.Peering, error) {
diff --git a/agent/rpc/peering/service_test.go b/agent/rpc/peering/service_test.go
index 405fe1a73..9ae1f6597 100644
--- a/agent/rpc/peering/service_test.go
+++ b/agent/rpc/peering/service_test.go
@@ -21,7 +21,9 @@ import (
 	"github.com/stretchr/testify/require"
 	gogrpc "google.golang.org/grpc"
 	"google.golang.org/grpc/codes"
+	"google.golang.org/grpc/metadata"
 	grpcstatus "google.golang.org/grpc/status"
+	"google.golang.org/protobuf/proto"
 
 	"github.com/hashicorp/consul/acl"
 	"github.com/hashicorp/consul/agent/connect"
@@ -861,6 +863,64 @@ func TestPeeringService_Read_ACLEnforcement(t *testing.T) {
 	}
 }
 
+func TestPeeringService_Read_Blocking(t *testing.T) {
+	// TODO(peering): see note on newTestServer, refactor to not use this
+	s := newTestServer(t, nil)
+
+	// insert peering directly to state store
+	lastIdx := uint64(10)
+	p := &pbpeering.Peering{
+		ID:                  testUUID(t),
+		Name:                "foo",
+		State:               pbpeering.PeeringState_ESTABLISHING,
+		PeerCAPems:          nil,
+		PeerServerName:      "test",
+		PeerServerAddresses: []string{"addr1"},
+	}
+	err := s.Server.FSM().State().PeeringWrite(lastIdx, &pbpeering.PeeringWriteRequest{Peering: p})
+	require.NoError(t, err)
+
+	client := pbpeering.NewPeeringServiceClient(s.ClientConn(t))
+
+	// Setup blocking query
+	ctx, cancel := context.WithTimeout(context.Background(), 10*time.Second)
+	t.Cleanup(cancel)
+
+	options := structs.QueryOptions{
+		MinQueryIndex: lastIdx,
+		MaxQueryTime:  1 * time.Second,
+	}
+	ctx, err = external.ContextWithQueryOptions(ctx, options)
+	require.NoError(t, err)
+
+	// Mutate the original peering
+	p = proto.Clone(p).(*pbpeering.Peering)
+	p.PeerServerAddresses = append(p.PeerServerAddresses, "addr2")
+
+	// Async change to trigger update
+	marker := time.Now()
+	go func() {
+		time.Sleep(100 * time.Millisecond)
+		lastIdx++
+		require.NoError(t, s.Server.FSM().State().PeeringWrite(lastIdx, &pbpeering.PeeringWriteRequest{Peering: p}))
+	}()
+
+	var header metadata.MD
+	resp, err := client.PeeringRead(ctx, &pbpeering.PeeringReadRequest{Name: "foo"}, gogrpc.Header(&header))
+	require.NoError(t, err)
+
+	// The query should return after the async change, but before the timeout
+	require.True(t, time.Since(marker) >= 100*time.Millisecond)
+	require.True(t, time.Since(marker) < 1*time.Second)
+
+	// Verify query results
+	meta, err := external.QueryMetaFromGRPCMeta(header)
+	require.NoError(t, err)
+	require.Equal(t, lastIdx, meta.Index)
+
+	prototest.AssertDeepEqual(t, p, resp.Peering)
+}
+
 func TestPeeringService_Delete(t *testing.T) {
 	tt := map[string]pbpeering.PeeringState{
 		"active peering":     pbpeering.PeeringState_ACTIVE,
@@ -993,6 +1053,7 @@ func TestPeeringService_List(t *testing.T) {
 	// Insert peerings directly to state store.
 	// Note that the state store holds reference to the underlying
 	// variables; do not modify them after writing.
+	lastIdx := uint64(10)
 	foo := &pbpeering.Peering{
 		ID:                  testUUID(t),
 		Name:                "foo",
@@ -1001,7 +1062,9 @@ func TestPeeringService_List(t *testing.T) {
 		PeerServerName:      "fooservername",
 		PeerServerAddresses: []string{"addr1"},
 	}
-	require.NoError(t, s.Server.FSM().State().PeeringWrite(10, &pbpeering.PeeringWriteRequest{Peering: foo}))
+	require.NoError(t, s.Server.FSM().State().PeeringWrite(lastIdx, &pbpeering.PeeringWriteRequest{Peering: foo}))
+
+	lastIdx++
 	bar := &pbpeering.Peering{
 		ID:                  testUUID(t),
 		Name:                "bar",
@@ -1010,21 +1073,78 @@ func TestPeeringService_List(t *testing.T) {
 		PeerServerName:      "barservername",
 		PeerServerAddresses: []string{"addr1"},
 	}
-	require.NoError(t, s.Server.FSM().State().PeeringWrite(15, &pbpeering.PeeringWriteRequest{Peering: bar}))
+	require.NoError(t, s.Server.FSM().State().PeeringWrite(lastIdx, &pbpeering.PeeringWriteRequest{Peering: bar}))
 
 	client := pbpeering.NewPeeringServiceClient(s.ClientConn(t))
 
-	ctx, cancel := context.WithTimeout(context.Background(), 10*time.Second)
-	t.Cleanup(cancel)
+	t.Run("non-blocking query", func(t *testing.T) {
+		ctx, cancel := context.WithTimeout(context.Background(), 10*time.Second)
+		t.Cleanup(cancel)
 
-	resp, err := client.PeeringList(ctx, &pbpeering.PeeringListRequest{})
-	require.NoError(t, err)
+		var header metadata.MD
+		resp, err := client.PeeringList(ctx, &pbpeering.PeeringListRequest{}, gogrpc.Header(&header))
+		require.NoError(t, err)
 
-	expect := &pbpeering.PeeringListResponse{
-		Peerings: []*pbpeering.Peering{bar, foo},
-		Index:    15,
-	}
-	prototest.AssertDeepEqual(t, expect, resp)
+		meta, err := external.QueryMetaFromGRPCMeta(header)
+		require.NoError(t, err)
+		require.Equal(t, lastIdx, meta.Index)
+
+		expect := &pbpeering.PeeringListResponse{
+			Peerings:       []*pbpeering.Peering{bar, foo},
+			OBSOLETE_Index: lastIdx,
+		}
+		prototest.AssertDeepEqual(t, expect, resp)
+	})
+
+	t.Run("blocking query", func(t *testing.T) {
+		// Setup blocking query
+		ctx, cancel := context.WithTimeout(context.Background(), 10*time.Second)
+		t.Cleanup(cancel)
+
+		marker := time.Now()
+		options := structs.QueryOptions{
+			MinQueryIndex: lastIdx,
+			MaxQueryTime:  1 * time.Second,
+		}
+		ctx, err := external.ContextWithQueryOptions(ctx, options)
+		require.NoError(t, err)
+
+		// Async change to trigger update
+		baz := &pbpeering.Peering{
+			ID:                  testUUID(t),
+			Name:                "baz",
+			State:               pbpeering.PeeringState_ACTIVE,
+			PeerCAPems:          nil,
+			PeerServerName:      "bazservername",
+			PeerServerAddresses: []string{"addr1"},
+		}
+		go func() {
+			time.Sleep(100 * time.Millisecond)
+
+			lastIdx++
+			require.NoError(t, s.Server.FSM().State().PeeringWrite(lastIdx, &pbpeering.PeeringWriteRequest{Peering: baz}))
+		}()
+
+		// Make the blocking query
+		var header metadata.MD
+		resp, err := client.PeeringList(ctx, &pbpeering.PeeringListRequest{}, gogrpc.Header(&header))
+		require.NoError(t, err)
+
+		// The query should return after the async change, but before the timeout
+		require.True(t, time.Since(marker) >= 100*time.Millisecond)
+		require.True(t, time.Since(marker) < 1*time.Second)
+
+		// Verify query results
+		meta, err := external.QueryMetaFromGRPCMeta(header)
+		require.NoError(t, err)
+		require.Equal(t, lastIdx, meta.Index)
+
+		expect := &pbpeering.PeeringListResponse{
+			Peerings:       []*pbpeering.Peering{bar, baz, foo},
+			OBSOLETE_Index: lastIdx,
+		}
+		prototest.AssertDeepEqual(t, expect, resp)
+	})
 }
 
 func TestPeeringService_List_ACLEnforcement(t *testing.T) {
@@ -1087,8 +1207,8 @@ func TestPeeringService_List_ACLEnforcement(t *testing.T) {
 			name:  "read token grants permission",
 			token: testTokenPeeringReadSecret,
 			expect: &pbpeering.PeeringListResponse{
-				Peerings: []*pbpeering.Peering{bar, foo},
-				Index:    15,
+				Peerings:       []*pbpeering.Peering{bar, foo},
+				OBSOLETE_Index: 15,
 			},
 		},
 	}
@@ -1115,16 +1235,65 @@ func TestPeeringService_TrustBundleRead(t *testing.T) {
 	lastIdx++
 	require.NoError(t, store.PeeringTrustBundleWrite(lastIdx, bundle))
 
-	ctx, cancel := context.WithCancel(context.Background())
-	defer cancel()
+	t.Run("non-blocking query", func(t *testing.T) {
+		ctx, cancel := context.WithTimeout(context.Background(), 10*time.Second)
+		t.Cleanup(cancel)
 
-	resp, err := client.TrustBundleRead(ctx, &pbpeering.TrustBundleReadRequest{
-		Name: "my-peering",
+		resp, err := client.TrustBundleRead(ctx, &pbpeering.TrustBundleReadRequest{
+			Name: "my-peering",
+		})
+		require.NoError(t, err)
+		require.Equal(t, lastIdx, resp.OBSOLETE_Index)
+		require.NotNil(t, resp.Bundle)
+		prototest.AssertDeepEqual(t, bundle, resp.Bundle)
+	})
+
+	t.Run("blocking query", func(t *testing.T) {
+		// Set up the blocking query
+		ctx, cancel := context.WithTimeout(context.Background(), 10*time.Second)
+		t.Cleanup(cancel)
+
+		marker := time.Now()
+		options := structs.QueryOptions{
+			MinQueryIndex: lastIdx,
+			MaxQueryTime:  1 * time.Second,
+		}
+		ctx, err := external.ContextWithQueryOptions(ctx, options)
+		require.NoError(t, err)
+
+		updatedBundle := &pbpeering.PeeringTrustBundle{
+			TrustDomain: "peer1.com",
+			PeerName:    "my-peering",
+			RootPEMs:    []string{"peer1-root-1", "peer1-root-2"}, // Adding a CA here
+		}
+
+		// Async change to trigger update
+		go func() {
+			time.Sleep(100 * time.Millisecond)
+			lastIdx++
+			require.NoError(t, store.PeeringTrustBundleWrite(lastIdx, updatedBundle))
+		}()
+
+		// Make the blocking query
+		var header metadata.MD
+		resp, err := client.TrustBundleRead(ctx, &pbpeering.TrustBundleReadRequest{
+			Name: "my-peering",
+		}, gogrpc.Header(&header))
+		require.NoError(t, err)
+
+		// The query should return after the async change, but before the timeout
+		require.True(t, time.Since(marker) >= 100*time.Millisecond)
+		require.True(t, time.Since(marker) < 1*time.Second)
+
+		// Verify query results
+		meta, err := external.QueryMetaFromGRPCMeta(header)
+		require.NoError(t, err)
+		require.Equal(t, lastIdx, meta.Index)
+
+		require.Equal(t, lastIdx, resp.OBSOLETE_Index)
+		require.NotNil(t, resp.Bundle)
+		prototest.AssertDeepEqual(t, updatedBundle, resp.Bundle)
 	})
-	require.NoError(t, err)
-	require.Equal(t, lastIdx, resp.Index)
-	require.NotNil(t, resp.Bundle)
-	prototest.AssertDeepEqual(t, bundle, resp.Bundle)
 }
 
 func TestPeeringService_TrustBundleRead_ACLEnforcement(t *testing.T) {
@@ -1290,14 +1459,64 @@ func TestPeeringService_TrustBundleListByService(t *testing.T) {
 
 	client := pbpeering.NewPeeringServiceClient(s.ClientConn(t))
 
-	req := pbpeering.TrustBundleListByServiceRequest{
-		ServiceName: "api",
-	}
-	resp, err := client.TrustBundleListByService(context.Background(), &req)
-	require.NoError(t, err)
-	require.Len(t, resp.Bundles, 2)
-	require.Equal(t, []string{"bar-root-1"}, resp.Bundles[0].RootPEMs)
-	require.Equal(t, []string{"foo-root-1"}, resp.Bundles[1].RootPEMs)
+	t.Run("non-blocking query", func(t *testing.T) {
+		req := pbpeering.TrustBundleListByServiceRequest{
+			ServiceName: "api",
+		}
+		resp, err := client.TrustBundleListByService(context.Background(), &req)
+		require.NoError(t, err)
+		require.Len(t, resp.Bundles, 2)
+		require.Equal(t, []string{"bar-root-1"}, resp.Bundles[0].RootPEMs)
+		require.Equal(t, []string{"foo-root-1"}, resp.Bundles[1].RootPEMs)
+		require.Equal(t, uint64(17), resp.OBSOLETE_Index)
+	})
+
+	t.Run("blocking query", func(t *testing.T) {
+		// Setup blocking query
+		ctx, cancel := context.WithTimeout(context.Background(), 10*time.Second)
+		t.Cleanup(cancel)
+
+		options := structs.QueryOptions{
+			MinQueryIndex: lastIdx,
+			MaxQueryTime:  1 * time.Second,
+		}
+		ctx, err := external.ContextWithQueryOptions(ctx, options)
+		require.NoError(t, err)
+
+		// Async change to trigger update
+		marker := time.Now()
+		go func() {
+			time.Sleep(100 * time.Millisecond)
+			lastIdx++
+			require.NoError(t, store.PeeringTrustBundleWrite(lastIdx, &pbpeering.PeeringTrustBundle{
+				TrustDomain: "bar.com",
+				PeerName:    "bar",
+				RootPEMs:    []string{"bar-root-1", "bar-root-2"}, // Appending new cert
+			}))
+		}()
+
+		// Make the blocking query
+		req := pbpeering.TrustBundleListByServiceRequest{
+			ServiceName: "api",
+		}
+		var header metadata.MD
+		resp, err := client.TrustBundleListByService(ctx, &req, gogrpc.Header(&header))
+		require.NoError(t, err)
+
+		// The query should return after the async change, but before the timeout
+		require.True(t, time.Since(marker) >= 100*time.Millisecond)
+		require.True(t, time.Since(marker) < 1*time.Second)
+
+		// Verify query results
+		meta, err := external.QueryMetaFromGRPCMeta(header)
+		require.NoError(t, err)
+		require.Equal(t, uint64(18), meta.Index)
+
+		require.Len(t, resp.Bundles, 2)
+		require.Equal(t, []string{"bar-root-1", "bar-root-2"}, resp.Bundles[0].RootPEMs)
+		require.Equal(t, []string{"foo-root-1"}, resp.Bundles[1].RootPEMs)
+		require.Equal(t, uint64(18), resp.OBSOLETE_Index)
+	})
 }
 
 func TestPeeringService_validatePeer(t *testing.T) {
diff --git a/agent/structs/structs.go b/agent/structs/structs.go
index f36a5b77c..ab8f54e97 100644
--- a/agent/structs/structs.go
+++ b/agent/structs/structs.go
@@ -420,6 +420,17 @@ func (q QueryBackend) String() string {
 	}
 }
 
+func QueryBackendFromString(s string) QueryBackend {
+	switch s {
+	case "blocking-query":
+		return QueryBackendBlocking
+	case "streaming":
+		return QueryBackendStreaming
+	default:
+		return QueryBackendBlocking
+	}
+}
+
 // QueryMeta allows a query response to include potentially
 // useful metadata about a query
 type QueryMeta struct {
diff --git a/agent/xds/testdata/clusters/mesh-gateway-with-peer-through-mesh-gateway-enabled.latest.golden b/agent/xds/testdata/clusters/mesh-gateway-with-peer-through-mesh-gateway-enabled.latest.golden
index 5b04edcac..805b3bccc 100644
--- a/agent/xds/testdata/clusters/mesh-gateway-with-peer-through-mesh-gateway-enabled.latest.golden
+++ b/agent/xds/testdata/clusters/mesh-gateway-with-peer-through-mesh-gateway-enabled.latest.golden
@@ -7,16 +7,25 @@
       "type": "EDS",
       "edsClusterConfig": {
         "edsConfig": {
-          "ads": {
-
-          },
+          "ads": {},
           "resourceApiVersion": "V3"
         }
       },
       "connectTimeout": "5s",
-      "outlierDetection": {
-
-      }
+      "outlierDetection": {}
+    },
+    {
+      "@type": "type.googleapis.com/envoy.config.cluster.v3.Cluster",
+      "name": "server.dc2.peering.f3f41279-001d-42bb-912e-f6103fb036b8",
+      "type": "EDS",
+      "edsClusterConfig": {
+        "edsConfig": {
+          "ads": {},
+          "resourceApiVersion": "V3"
+        }
+      },
+      "connectTimeout": "5s",
+      "outlierDetection": {}
     },
     {
       "@type": "type.googleapis.com/envoy.config.cluster.v3.Cluster",
@@ -44,9 +53,7 @@
       },
       "dnsRefreshRate": "10s",
       "dnsLookupFamily": "V4_ONLY",
-      "outlierDetection": {
-
-      }
+      "outlierDetection": {}
     }
   ],
   "typeUrl": "type.googleapis.com/envoy.config.cluster.v3.Cluster",
diff --git a/agent/xds/testdata/endpoints/mesh-gateway-with-peer-through-mesh-gateway-enabled.latest.golden b/agent/xds/testdata/endpoints/mesh-gateway-with-peer-through-mesh-gateway-enabled.latest.golden
index 475659df2..2f88c1fb5 100644
--- a/agent/xds/testdata/endpoints/mesh-gateway-with-peer-through-mesh-gateway-enabled.latest.golden
+++ b/agent/xds/testdata/endpoints/mesh-gateway-with-peer-through-mesh-gateway-enabled.latest.golden
@@ -30,6 +30,26 @@
           ]
         }
       ]
+    },
+    {
+      "@type": "type.googleapis.com/envoy.config.endpoint.v3.ClusterLoadAssignment",
+      "clusterName": "server.dc2.peering.f3f41279-001d-42bb-912e-f6103fb036b8",
+      "endpoints": [
+        {
+          "lbEndpoints": [
+            {
+              "endpoint": {
+                "address": {
+                  "socketAddress": {
+                    "address": "1.2.3.4",
+                    "portValue": 5200
+                  }
+                }
+              }
+            }
+          ]
+        }
+      ]
     }
   ],
   "typeUrl": "type.googleapis.com/envoy.config.endpoint.v3.ClusterLoadAssignment",
diff --git a/agent/xds/testdata/listeners/mesh-gateway-with-peer-through-mesh-gateway-enabled.latest.golden b/agent/xds/testdata/listeners/mesh-gateway-with-peer-through-mesh-gateway-enabled.latest.golden
index eba604091..faae8d00d 100644
--- a/agent/xds/testdata/listeners/mesh-gateway-with-peer-through-mesh-gateway-enabled.latest.golden
+++ b/agent/xds/testdata/listeners/mesh-gateway-with-peer-through-mesh-gateway-enabled.latest.golden
@@ -28,6 +28,23 @@
             }
           ]
         },
+        {
+          "filterChainMatch": {
+            "serverNames": [
+              "server.dc2.peering.f3f41279-001d-42bb-912e-f6103fb036b8"
+            ]
+          },
+          "filters": [
+            {
+              "name": "envoy.filters.network.tcp_proxy",
+              "typedConfig": {
+                "@type": "type.googleapis.com/envoy.extensions.filters.network.tcp_proxy.v3.TcpProxy",
+                "statPrefix": "mesh_gateway_remote_peering_servers.server.dc2.peering.f3f41279-001d-42bb-912e-f6103fb036b8",
+                "cluster": "server.dc2.peering.f3f41279-001d-42bb-912e-f6103fb036b8"
+              }
+            }
+          ]
+        },
         {
           "filterChainMatch": {
             "serverNames": [
diff --git a/internal/tools/proto-gen-rpc-glue/e2e/source.pb.go b/internal/tools/proto-gen-rpc-glue/e2e/source.pb.go
index e64455cd1..3a83b8431 100644
--- a/internal/tools/proto-gen-rpc-glue/e2e/source.pb.go
+++ b/internal/tools/proto-gen-rpc-glue/e2e/source.pb.go
@@ -41,21 +41,6 @@ type ExampleDatacenter struct {
 	Datacenter string
 }
 
-// @consul-rpc-glue: ReadTODO
-type ExampleReadTODO struct {
-	Value string
-}
-
-// @consul-rpc-glue: LeaderReadTODO
-type ExampleLeaderReadTODO struct {
-	Value string
-}
-
-// @consul-rpc-glue: WriteTODO
-type ExampleWriteTODO struct {
-	Value string
-}
-
 // @consul-rpc-glue: WriteRequest=AltWriteRequest
 type AltExampleWriteRequest struct {
 	Value           int
diff --git a/internal/tools/proto-gen-rpc-glue/e2e/source.rpcglue.pb.go.golden b/internal/tools/proto-gen-rpc-glue/e2e/source.rpcglue.pb.go.golden
index 4c7b1c361..92ee7c682 100644
--- a/internal/tools/proto-gen-rpc-glue/e2e/source.rpcglue.pb.go.golden
+++ b/internal/tools/proto-gen-rpc-glue/e2e/source.rpcglue.pb.go.golden
@@ -1,6 +1,3 @@
-//go:build example
-// +build example
-
 // Code generated by proto-gen-rpc-glue. DO NOT EDIT.
 
 package e2e
@@ -28,14 +25,6 @@ func (msg *ExampleWriteRequest) HasTimedOut(start time.Time, rpcHoldTimeout time
 	return msg.WriteRequest.HasTimedOut(start, rpcHoldTimeout, a, b)
 }
 
-// Timeout implements structs.RPCInfo
-func (msg *ExampleWriteRequest) Timeout(rpcHoldTimeout time.Duration, a time.Duration, b time.Duration) time.Duration {
-	if msg == nil || msg.WriteRequest == nil {
-		return 0
-	}
-	return msg.WriteRequest.Timeout(rpcHoldTimeout, a, b)
-}
-
 // IsRead implements structs.RPCInfo
 func (msg *ExampleWriteRequest) IsRead() bool {
 	return false
@@ -90,14 +79,6 @@ func (msg *ExampleReadRequest) HasTimedOut(start time.Time, rpcHoldTimeout time.
 	return msg.ReadRequest.HasTimedOut(start, rpcHoldTimeout, a, b)
 }
 
-// Timeout implements structs.RPCInfo
-func (msg *ExampleReadRequest) Timeout(rpcHoldTimeout time.Duration, a time.Duration, b time.Duration) time.Duration {
-	if msg == nil || msg.ReadRequest == nil {
-		return 0
-	}
-	return msg.ReadRequest.Timeout(rpcHoldTimeout, a, b)
-}
-
 // SetTokenSecret implements structs.RPCInfo
 func (msg *ExampleReadRequest) SetTokenSecret(s string) {
 	// TODO: initialize if nil
@@ -146,6 +127,16 @@ func (msg *ExampleQueryOptions) AllowStaleRead() bool {
 	return msg.QueryOptions.AllowStaleRead()
 }
 
+// BlockingTimeout implements pool.BlockableQuery
+func (msg *ExampleQueryOptions) BlockingTimeout(maxQueryTime, defaultQueryTime time.Duration) time.Duration {
+	maxTime := structs.DurationFromProto(msg.QueryOptions.GetMaxQueryTime())
+	o := structs.QueryOptions{
+		MaxQueryTime:  maxTime,
+		MinQueryIndex: msg.QueryOptions.GetMinQueryIndex(),
+	}
+	return o.BlockingTimeout(maxQueryTime, defaultQueryTime)
+}
+
 // HasTimedOut implements structs.RPCInfo
 func (msg *ExampleQueryOptions) HasTimedOut(start time.Time, rpcHoldTimeout time.Duration, a time.Duration, b time.Duration) (bool, error) {
 	if msg == nil || msg.QueryOptions == nil {
@@ -154,14 +145,6 @@ func (msg *ExampleQueryOptions) HasTimedOut(start time.Time, rpcHoldTimeout time
 	return msg.QueryOptions.HasTimedOut(start, rpcHoldTimeout, a, b)
 }
 
-// Timeout implements structs.RPCInfo
-func (msg *ExampleQueryOptions) Timeout(rpcHoldTimeout time.Duration, a time.Duration, b time.Duration) time.Duration {
-	if msg == nil || msg.QueryOptions == nil {
-		return 0
-	}
-	return msg.QueryOptions.Timeout(rpcHoldTimeout, a, b)
-}
-
 // SetTokenSecret implements structs.RPCInfo
 func (msg *ExampleQueryOptions) SetTokenSecret(s string) {
 	// TODO: initialize if nil
@@ -267,126 +250,6 @@ func (msg *ExampleDatacenter) RequestDatacenter() string {
 	return msg.Datacenter
 }
 
-// IsRead implements structs.RPCInfo
-func (msg *ExampleReadTODO) IsRead() bool {
-	// TODO(peering): figure out read semantics here
-	return true
-}
-
-// AllowStaleRead implements structs.RPCInfo
-func (msg *ExampleReadTODO) AllowStaleRead() bool {
-	// TODO(peering): figure out read semantics here
-	return false
-}
-
-// HasTimedOut implements structs.RPCInfo
-func (msg *ExampleReadTODO) HasTimedOut(start time.Time, rpcHoldTimeout time.Duration, a time.Duration, b time.Duration) (bool, error) {
-	// TODO(peering): figure out read semantics here
-	return time.Since(start) > rpcHoldTimeout, nil
-}
-
-// Timeout implements structs.RPCInfo
-func (msg *ExampleReadTODO) Timeout(rpcHoldTimeout time.Duration, a time.Duration, b time.Duration) time.Duration {
-	// TODO(peering): figure out read semantics here
-	return rpcHoldTimeout
-}
-
-// SetTokenSecret implements structs.RPCInfo
-func (msg *ExampleReadTODO) SetTokenSecret(s string) {
-	// TODO(peering): figure out read semantics here
-}
-
-// TokenSecret implements structs.RPCInfo
-func (msg *ExampleReadTODO) TokenSecret() string {
-	// TODO(peering): figure out read semantics here
-	return ""
-}
-
-// Token implements structs.RPCInfo
-func (msg *ExampleReadTODO) Token() string {
-	// TODO(peering): figure out read semantics here
-	return ""
-}
-
-// IsRead implements structs.RPCInfo
-func (msg *ExampleLeaderReadTODO) IsRead() bool {
-	// TODO(peering): figure out read semantics here
-	return true
-}
-
-// AllowStaleRead implements structs.RPCInfo
-func (msg *ExampleLeaderReadTODO) AllowStaleRead() bool {
-	// TODO(peering): figure out read semantics here
-	// TODO(peering): this needs to stay false for calls to head to the leader until we sync stream tracker information
-	// like ImportedServicesCount, ExportedServicesCount, as well as general Status fields thru raft to make available
-	// to followers as well
-	return false
-}
-
-// HasTimedOut implements structs.RPCInfo
-func (msg *ExampleLeaderReadTODO) HasTimedOut(start time.Time, rpcHoldTimeout time.Duration, a time.Duration, b time.Duration) (bool, error) {
-	// TODO(peering): figure out read semantics here
-	return time.Since(start) > rpcHoldTimeout, nil
-}
-
-// Timeout implements structs.RPCInfo
-func (msg *ExampleLeaderReadTODO) Timeout(rpcHoldTimeout time.Duration, a time.Duration, b time.Duration) time.Duration {
-	// TODO(peering): figure out read semantics here
-	return rpcHoldTimeout
-}
-
-// SetTokenSecret implements structs.RPCInfo
-func (msg *ExampleLeaderReadTODO) SetTokenSecret(s string) {
-	// TODO(peering): figure out read semantics here
-}
-
-// TokenSecret implements structs.RPCInfo
-func (msg *ExampleLeaderReadTODO) TokenSecret() string {
-	// TODO(peering): figure out read semantics here
-	return ""
-}
-
-// Token implements structs.RPCInfo
-func (msg *ExampleLeaderReadTODO) Token() string {
-	// TODO(peering): figure out read semantics here
-	return ""
-}
-
-// IsRead implements structs.RPCInfo
-func (msg *ExampleWriteTODO) IsRead() bool {
-	// TODO(peering): figure out write semantics here
-	return false
-}
-
-// AllowStaleRead implements structs.RPCInfo
-func (msg *ExampleWriteTODO) AllowStaleRead() bool {
-	// TODO(peering): figure out write semantics here
-	return false
-}
-
-// HasTimedOut implements structs.RPCInfo
-func (msg *ExampleWriteTODO) HasTimedOut(start time.Time, rpcHoldTimeout time.Duration, a time.Duration, b time.Duration) (bool, error) {
-	// TODO(peering): figure out write semantics here
-	return time.Since(start) > rpcHoldTimeout, nil
-}
-
-// Timeout implements structs.RPCInfo
-func (msg *ExampleWriteTODO) Timeout(rpcHoldTimeout time.Duration, a time.Duration, b time.Duration) time.Duration {
-	// TODO(peering): figure out write semantics here
-	return rpcHoldTimeout
-}
-
-// SetTokenSecret implements structs.RPCInfo
-func (msg *ExampleWriteTODO) SetTokenSecret(s string) {
-	// TODO(peering): figure out write semantics here
-}
-
-// TokenSecret implements structs.RPCInfo
-func (msg *ExampleWriteTODO) TokenSecret() string {
-	// TODO(peering): figure out write semantics here
-	return ""
-}
-
 // AllowStaleRead implements structs.RPCInfo
 func (msg *AltExampleWriteRequest) AllowStaleRead() bool {
 	return false
@@ -400,14 +263,6 @@ func (msg *AltExampleWriteRequest) HasTimedOut(start time.Time, rpcHoldTimeout t
 	return msg.AltWriteRequest.HasTimedOut(start, rpcHoldTimeout, a, b)
 }
 
-// Timeout implements structs.RPCInfo
-func (msg *AltExampleWriteRequest) Timeout(rpcHoldTimeout time.Duration, a time.Duration, b time.Duration) time.Duration {
-	if msg == nil || msg.AltWriteRequest == nil {
-		return 0
-	}
-	return msg.AltWriteRequest.Timeout(rpcHoldTimeout, a, b)
-}
-
 // IsRead implements structs.RPCInfo
 func (msg *AltExampleWriteRequest) IsRead() bool {
 	return false
@@ -454,14 +309,6 @@ func (msg *AltExampleReadRequest) HasTimedOut(start time.Time, rpcHoldTimeout ti
 	return msg.AltReadRequest.HasTimedOut(start, rpcHoldTimeout, a, b)
 }
 
-// Timeout implements structs.RPCInfo
-func (msg *AltExampleReadRequest) Timeout(rpcHoldTimeout time.Duration, a time.Duration, b time.Duration) time.Duration {
-	if msg == nil || msg.AltReadRequest == nil {
-		return 0
-	}
-	return msg.AltReadRequest.Timeout(rpcHoldTimeout, a, b)
-}
-
 // SetTokenSecret implements structs.RPCInfo
 func (msg *AltExampleReadRequest) SetTokenSecret(s string) {
 	// TODO: initialize if nil
@@ -494,6 +341,16 @@ func (msg *AltExampleQueryOptions) AllowStaleRead() bool {
 	return msg.AltQueryOptions.AllowStaleRead()
 }
 
+// BlockingTimeout implements pool.BlockableQuery
+func (msg *AltExampleQueryOptions) BlockingTimeout(maxQueryTime, defaultQueryTime time.Duration) time.Duration {
+	maxTime := structs.DurationFromProto(msg.AltQueryOptions.GetMaxQueryTime())
+	o := structs.QueryOptions{
+		MaxQueryTime:  maxTime,
+		MinQueryIndex: msg.AltQueryOptions.GetMinQueryIndex(),
+	}
+	return o.BlockingTimeout(maxQueryTime, defaultQueryTime)
+}
+
 // HasTimedOut implements structs.RPCInfo
 func (msg *AltExampleQueryOptions) HasTimedOut(start time.Time, rpcHoldTimeout time.Duration, a time.Duration, b time.Duration) (bool, error) {
 	if msg == nil || msg.AltQueryOptions == nil {
@@ -502,14 +359,6 @@ func (msg *AltExampleQueryOptions) HasTimedOut(start time.Time, rpcHoldTimeout t
 	return msg.AltQueryOptions.HasTimedOut(start, rpcHoldTimeout, a, b)
 }
 
-// Timeout implements structs.RPCInfo
-func (msg *AltExampleQueryOptions) Timeout(rpcHoldTimeout time.Duration, a time.Duration, b time.Duration) time.Duration {
-	if msg == nil || msg.AltQueryOptions == nil {
-		return 0
-	}
-	return msg.AltQueryOptions.Timeout(rpcHoldTimeout, a, b)
-}
-
 // SetTokenSecret implements structs.RPCInfo
 func (msg *AltExampleQueryOptions) SetTokenSecret(s string) {
 	// TODO: initialize if nil
diff --git a/internal/tools/proto-gen-rpc-glue/main.go b/internal/tools/proto-gen-rpc-glue/main.go
index b9ac7d7a9..65a25122b 100644
--- a/internal/tools/proto-gen-rpc-glue/main.go
+++ b/internal/tools/proto-gen-rpc-glue/main.go
@@ -108,15 +108,6 @@ func processFile(path string) error {
 			if ann.Datacenter != "" {
 				log.Printf("    Datacenter from %s", ann.Datacenter)
 			}
-			if ann.ReadTODO != "" {
-				log.Printf("    ReadTODO from %s", ann.ReadTODO)
-			}
-			if ann.LeaderReadTODO != "" {
-				log.Printf("    LeaderReadTODO from %s", ann.LeaderReadTODO)
-			}
-			if ann.WriteTODO != "" {
-				log.Printf("    WriteTODO from %s", ann.WriteTODO)
-			}
 		}
 	}
 
@@ -163,15 +154,6 @@ var _ time.Month
 		if typ.Annotation.Datacenter != "" {
 			buf.WriteString(fmt.Sprintf(tmplDatacenter, typ.Name, typ.Annotation.Datacenter))
 		}
-		if typ.Annotation.LeaderReadTODO != "" {
-			buf.WriteString(fmt.Sprintf(tmplLeaderOnlyReadTODO, typ.Name, typ.Annotation.LeaderReadTODO))
-		}
-		if typ.Annotation.ReadTODO != "" {
-			buf.WriteString(fmt.Sprintf(tmplReadTODO, typ.Name, typ.Annotation.ReadTODO))
-		}
-		if typ.Annotation.WriteTODO != "" {
-			buf.WriteString(fmt.Sprintf(tmplWriteTODO, typ.Name, typ.Annotation.WriteTODO))
-		}
 	}
 
 	// write to disk
@@ -325,13 +307,6 @@ func getAnnotation(doc []*ast.Comment) (Annotation, error) {
 		case strings.HasPrefix(part, "Datacenter="):
 			ann.Datacenter = strings.TrimPrefix(part, "Datacenter=")
 
-		case part == "ReadTODO":
-			ann.ReadTODO = "ReadTODO"
-		case part == "WriteTODO":
-			ann.WriteTODO = "WriteTODO"
-		case part == "LeaderReadTODO":
-			ann.LeaderReadTODO = "LeaderReadTODO"
-
 		default:
 			return Annotation{}, fmt.Errorf("unexpected annotation part: %s", part)
 		}
@@ -459,114 +434,6 @@ func (msg *%[1]s) Token() string {
 }
 `
 
-const tmplLeaderOnlyReadTODO = `
-// IsRead implements structs.RPCInfo
-func (msg *%[1]s) IsRead() bool {
-	// TODO(peering): figure out read semantics here
-	return true
-}
-
-// AllowStaleRead implements structs.RPCInfo
-func (msg *%[1]s) AllowStaleRead() bool {
-	// TODO(peering): figure out read semantics here
-	// TODO(peering): this needs to stay false for calls to head to the leader until we sync stream tracker information
-	// like ImportedServicesCount, ExportedServicesCount, as well as general Status fields thru raft to make available
-	// to followers as well
-	return false
-}
-
-// HasTimedOut implements structs.RPCInfo
-func (msg *%[1]s) HasTimedOut(start time.Time, rpcHoldTimeout time.Duration, a time.Duration, b time.Duration) (bool, error) {
-	// TODO(peering): figure out read semantics here
-	return time.Since(start) > rpcHoldTimeout, nil
-}
-
-// SetTokenSecret implements structs.RPCInfo
-func (msg *%[1]s) SetTokenSecret(s string) {
-	// TODO(peering): figure out read semantics here
-}
-
-// TokenSecret implements structs.RPCInfo
-func (msg *%[1]s) TokenSecret() string {
-	// TODO(peering): figure out read semantics here
-	return ""
-}
-
-// Token implements structs.RPCInfo
-func (msg *%[1]s) Token() string {
-	// TODO(peering): figure out read semantics here
-	return ""
-}
-`
-
-const tmplReadTODO = `
-// IsRead implements structs.RPCInfo
-func (msg *%[1]s) IsRead() bool {
-	// TODO(peering): figure out read semantics here
-	return true
-}
-
-// AllowStaleRead implements structs.RPCInfo
-func (msg *%[1]s) AllowStaleRead() bool {
-	// TODO(peering): figure out read semantics here
-	return false
-}
-
-// HasTimedOut implements structs.RPCInfo
-func (msg *%[1]s) HasTimedOut(start time.Time, rpcHoldTimeout time.Duration, a time.Duration, b time.Duration) (bool, error) {
-	// TODO(peering): figure out read semantics here
-	return time.Since(start) > rpcHoldTimeout, nil
-}
-
-// SetTokenSecret implements structs.RPCInfo
-func (msg *%[1]s) SetTokenSecret(s string) {
-	// TODO(peering): figure out read semantics here
-}
-
-// TokenSecret implements structs.RPCInfo
-func (msg *%[1]s) TokenSecret() string {
-	// TODO(peering): figure out read semantics here
-	return ""
-}
-
-// Token implements structs.RPCInfo
-func (msg *%[1]s) Token() string {
-	// TODO(peering): figure out read semantics here
-	return ""
-}
-`
-
-const tmplWriteTODO = `
-// IsRead implements structs.RPCInfo
-func (msg *%[1]s) IsRead() bool {
-	// TODO(peering): figure out write semantics here
-	return false
-}
-
-// AllowStaleRead implements structs.RPCInfo
-func (msg *%[1]s) AllowStaleRead() bool {
-	// TODO(peering): figure out write semantics here
-	return false
-}
-
-// HasTimedOut implements structs.RPCInfo
-func (msg *%[1]s) HasTimedOut(start time.Time, rpcHoldTimeout time.Duration, a time.Duration, b time.Duration) (bool, error) {
-	// TODO(peering): figure out write semantics here
-	return time.Since(start) > rpcHoldTimeout, nil
-}
-
-// SetTokenSecret implements structs.RPCInfo
-func (msg *%[1]s) SetTokenSecret(s string) {
-	// TODO(peering): figure out write semantics here
-}
-
-// TokenSecret implements structs.RPCInfo
-func (msg *%[1]s) TokenSecret() string {
-	// TODO(peering): figure out write semantics here
-	return ""
-}
-`
-
 const tmplTargetDatacenter = `
 // RequestDatacenter implements structs.RPCInfo
 func (msg *%[1]s) RequestDatacenter() string {
diff --git a/proto/private/pbpeering/peering.pb.go b/proto/private/pbpeering/peering.pb.go
index 308266634..82b88d1d7 100644
--- a/proto/private/pbpeering/peering.pb.go
+++ b/proto/private/pbpeering/peering.pb.go
@@ -792,7 +792,6 @@ func (x *PeeringServerAddresses) GetAddresses() []string {
 	return nil
 }
 
-// @consul-rpc-glue: LeaderReadTODO
 type PeeringReadRequest struct {
 	state         protoimpl.MessageState
 	sizeCache     protoimpl.SizeCache
@@ -895,7 +894,6 @@ func (x *PeeringReadResponse) GetPeering() *Peering {
 	return nil
 }
 
-// @consul-rpc-glue: LeaderReadTODO
 type PeeringListRequest struct {
 	state         protoimpl.MessageState
 	sizeCache     protoimpl.SizeCache
@@ -948,8 +946,8 @@ type PeeringListResponse struct {
 	sizeCache     protoimpl.SizeCache
 	unknownFields protoimpl.UnknownFields
 
-	Peerings []*Peering `protobuf:"bytes,1,rep,name=Peerings,proto3" json:"Peerings,omitempty"`
-	Index    uint64     `protobuf:"varint,2,opt,name=Index,proto3" json:"Index,omitempty"`
+	Peerings       []*Peering `protobuf:"bytes,1,rep,name=Peerings,proto3" json:"Peerings,omitempty"`
+	OBSOLETE_Index uint64     `protobuf:"varint,2,opt,name=OBSOLETE_Index,json=OBSOLETEIndex,proto3" json:"OBSOLETE_Index,omitempty"` // Deprecated in favor of gRPC metadata
 }
 
 func (x *PeeringListResponse) Reset() {
@@ -991,9 +989,9 @@ func (x *PeeringListResponse) GetPeerings() []*Peering {
 	return nil
 }
 
-func (x *PeeringListResponse) GetIndex() uint64 {
+func (x *PeeringListResponse) GetOBSOLETE_Index() uint64 {
 	if x != nil {
-		return x.Index
+		return x.OBSOLETE_Index
 	}
 	return 0
 }
@@ -1273,8 +1271,8 @@ type TrustBundleListByServiceResponse struct {
 	sizeCache     protoimpl.SizeCache
 	unknownFields protoimpl.UnknownFields
 
-	Index   uint64                `protobuf:"varint,1,opt,name=Index,proto3" json:"Index,omitempty"`
-	Bundles []*PeeringTrustBundle `protobuf:"bytes,2,rep,name=Bundles,proto3" json:"Bundles,omitempty"`
+	OBSOLETE_Index uint64                `protobuf:"varint,1,opt,name=OBSOLETE_Index,json=OBSOLETEIndex,proto3" json:"OBSOLETE_Index,omitempty"` // Deprecated in favor of gRPC metadata
+	Bundles        []*PeeringTrustBundle `protobuf:"bytes,2,rep,name=Bundles,proto3" json:"Bundles,omitempty"`
 }
 
 func (x *TrustBundleListByServiceResponse) Reset() {
@@ -1309,9 +1307,9 @@ func (*TrustBundleListByServiceResponse) Descriptor() ([]byte, []int) {
 	return file_private_pbpeering_peering_proto_rawDescGZIP(), []int{16}
 }
 
-func (x *TrustBundleListByServiceResponse) GetIndex() uint64 {
+func (x *TrustBundleListByServiceResponse) GetOBSOLETE_Index() uint64 {
 	if x != nil {
-		return x.Index
+		return x.OBSOLETE_Index
 	}
 	return 0
 }
@@ -1383,8 +1381,8 @@ type TrustBundleReadResponse struct {
 	sizeCache     protoimpl.SizeCache
 	unknownFields protoimpl.UnknownFields
 
-	Index  uint64              `protobuf:"varint,1,opt,name=Index,proto3" json:"Index,omitempty"`
-	Bundle *PeeringTrustBundle `protobuf:"bytes,2,opt,name=Bundle,proto3" json:"Bundle,omitempty"`
+	OBSOLETE_Index uint64              `protobuf:"varint,1,opt,name=OBSOLETE_Index,json=OBSOLETEIndex,proto3" json:"OBSOLETE_Index,omitempty"` // Deprecated in favor of gRPC metadata
+	Bundle         *PeeringTrustBundle `protobuf:"bytes,2,opt,name=Bundle,proto3" json:"Bundle,omitempty"`
 }
 
 func (x *TrustBundleReadResponse) Reset() {
@@ -1419,9 +1417,9 @@ func (*TrustBundleReadResponse) Descriptor() ([]byte, []int) {
 	return file_private_pbpeering_peering_proto_rawDescGZIP(), []int{18}
 }
 
-func (x *TrustBundleReadResponse) GetIndex() uint64 {
+func (x *TrustBundleReadResponse) GetOBSOLETE_Index() uint64 {
 	if x != nil {
-		return x.Index
+		return x.OBSOLETE_Index
 	}
 	return 0
 }
@@ -2485,234 +2483,237 @@ var file_private_pbpeering_peering_proto_rawDesc = []byte{
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 }
 
 var (
diff --git a/proto/private/pbpeering/peering.proto b/proto/private/pbpeering/peering.proto
index de460d798..098c8f638 100644
--- a/proto/private/pbpeering/peering.proto
+++ b/proto/private/pbpeering/peering.proto
@@ -322,7 +322,6 @@ message PeeringServerAddresses {
   repeated string Addresses = 1;
 }
 
-// @consul-rpc-glue: LeaderReadTODO
 message PeeringReadRequest {
   string Name = 1;
   string Partition = 2;
@@ -332,14 +331,13 @@ message PeeringReadResponse {
   Peering Peering = 1;
 }
 
-// @consul-rpc-glue: LeaderReadTODO
 message PeeringListRequest {
   string Partition = 1;
 }
 
 message PeeringListResponse {
   repeated Peering Peerings = 1;
-  uint64 Index = 2;
+  uint64 OBSOLETE_Index = 2; // Deprecated in favor of gRPC metadata
 }
 
 message PeeringWriteRequest {
@@ -373,7 +371,7 @@ message TrustBundleListByServiceRequest {
 }
 
 message TrustBundleListByServiceResponse {
-  uint64 Index = 1;
+  uint64 OBSOLETE_Index = 1; // Deprecated in favor of gRPC metadata
   repeated PeeringTrustBundle Bundles = 2;
 }
 
@@ -383,7 +381,7 @@ message TrustBundleReadRequest {
 }
 
 message TrustBundleReadResponse {
-  uint64 Index = 1;
+  uint64 OBSOLETE_Index = 1; // Deprecated in favor of gRPC metadata
   PeeringTrustBundle Bundle = 2;
 }
 
diff --git a/proto/private/pbpeering/peering.rpcglue.pb.go b/proto/private/pbpeering/peering.rpcglue.pb.go
deleted file mode 100644
index 1e6f94ce5..000000000
--- a/proto/private/pbpeering/peering.rpcglue.pb.go
+++ /dev/null
@@ -1,89 +0,0 @@
-// Code generated by proto-gen-rpc-glue. DO NOT EDIT.
-
-package pbpeering
-
-import (
-	"time"
-
-	"github.com/hashicorp/consul/agent/structs"
-)
-
-// Reference imports to suppress errors if they are not otherwise used.
-var _ structs.RPCInfo
-var _ time.Month
-
-// IsRead implements structs.RPCInfo
-func (msg *PeeringReadRequest) IsRead() bool {
-	// TODO(peering): figure out read semantics here
-	return true
-}
-
-// AllowStaleRead implements structs.RPCInfo
-func (msg *PeeringReadRequest) AllowStaleRead() bool {
-	// TODO(peering): figure out read semantics here
-	// TODO(peering): this needs to stay false for calls to head to the leader until we sync stream tracker information
-	// like ImportedServicesCount, ExportedServicesCount, as well as general Status fields thru raft to make available
-	// to followers as well
-	return false
-}
-
-// HasTimedOut implements structs.RPCInfo
-func (msg *PeeringReadRequest) HasTimedOut(start time.Time, rpcHoldTimeout time.Duration, a time.Duration, b time.Duration) (bool, error) {
-	// TODO(peering): figure out read semantics here
-	return time.Since(start) > rpcHoldTimeout, nil
-}
-
-// SetTokenSecret implements structs.RPCInfo
-func (msg *PeeringReadRequest) SetTokenSecret(s string) {
-	// TODO(peering): figure out read semantics here
-}
-
-// TokenSecret implements structs.RPCInfo
-func (msg *PeeringReadRequest) TokenSecret() string {
-	// TODO(peering): figure out read semantics here
-	return ""
-}
-
-// Token implements structs.RPCInfo
-func (msg *PeeringReadRequest) Token() string {
-	// TODO(peering): figure out read semantics here
-	return ""
-}
-
-// IsRead implements structs.RPCInfo
-func (msg *PeeringListRequest) IsRead() bool {
-	// TODO(peering): figure out read semantics here
-	return true
-}
-
-// AllowStaleRead implements structs.RPCInfo
-func (msg *PeeringListRequest) AllowStaleRead() bool {
-	// TODO(peering): figure out read semantics here
-	// TODO(peering): this needs to stay false for calls to head to the leader until we sync stream tracker information
-	// like ImportedServicesCount, ExportedServicesCount, as well as general Status fields thru raft to make available
-	// to followers as well
-	return false
-}
-
-// HasTimedOut implements structs.RPCInfo
-func (msg *PeeringListRequest) HasTimedOut(start time.Time, rpcHoldTimeout time.Duration, a time.Duration, b time.Duration) (bool, error) {
-	// TODO(peering): figure out read semantics here
-	return time.Since(start) > rpcHoldTimeout, nil
-}
-
-// SetTokenSecret implements structs.RPCInfo
-func (msg *PeeringListRequest) SetTokenSecret(s string) {
-	// TODO(peering): figure out read semantics here
-}
-
-// TokenSecret implements structs.RPCInfo
-func (msg *PeeringListRequest) TokenSecret() string {
-	// TODO(peering): figure out read semantics here
-	return ""
-}
-
-// Token implements structs.RPCInfo
-func (msg *PeeringListRequest) Token() string {
-	// TODO(peering): figure out read semantics here
-	return ""
-}
diff --git a/website/content/api-docs/peering.mdx b/website/content/api-docs/peering.mdx
index a6afb29d8..9478af104 100644
--- a/website/content/api-docs/peering.mdx
+++ b/website/content/api-docs/peering.mdx
@@ -154,7 +154,7 @@ The table below shows this endpoint's support for
 
 | Blocking Queries | Consistency Modes | Agent Caching | ACL Required   |
 | ---------------- | ----------------- | ------------- | -------------- |
-| `NO`             | `consistent`      | `none`        | `peering:read` |
+| `YES`            | `consistent`      | `none`        | `peering:read` |
 
 ### Path Parameters
 
@@ -263,9 +263,9 @@ The table below shows this endpoint's support for
 [agent caching](/consul/api-docs/features/caching), and
 [required ACLs](/consul/api-docs/api-structure#authentication).
 
-| Blocking Queries | Consistency Modes | Agent Caching | ACL Required   |
-| ---------------- | ----------------- | ------------- | -------------- |
-| `NO`             | `consistent`      | `none`        | `peering:read` |
+| Blocking Queries | Consistency Modes | Agent Caching        | ACL Required   |
+| ---------------- | ----------------- | -------------------- | -------------- |
+| `YES`            | `consistent`      | `background refresh` | `peering:read` |
 
 ### Query Parameters