diff --git a/builtin/logical/pki/acme_challenge_engine.go b/builtin/logical/pki/acme_challenge_engine.go
index 71ade368f..7dae884ca 100644
--- a/builtin/logical/pki/acme_challenge_engine.go
+++ b/builtin/logical/pki/acme_challenge_engine.go
@@ -10,6 +10,7 @@ import (
 	"sync"
 	"time"
 
+	"github.com/hashicorp/vault/sdk/helper/consts"
 	"github.com/hashicorp/vault/sdk/logical"
 )
 
@@ -42,6 +43,7 @@ type ChallengeValidation struct {
 type ChallengeQueueEntry struct {
 	Identifier string
 	RetryAfter time.Time
+	NumRetries int // Track if we are spinning on a corrupted challenge
 }
 
 type ACMEChallengeEngine struct {
@@ -97,7 +99,7 @@ func (ace *ACMEChallengeEngine) Run(b *backend, state *acmeState, sc *storageCon
 		b.Logger().Error("failed loading existing ACME challenge validations:", "err", err)
 	}
 
-	for true {
+	for {
 		// err == nil on shutdown.
 		b.Logger().Debug("Starting ACME challenge validation engine")
 		err := ace._run(b, state)
@@ -119,7 +121,7 @@ func (ace *ACMEChallengeEngine) _run(b *backend, state *acmeState) error {
 	// We want at most a certain number of workers operating to verify
 	// challenges.
 	var finishedWorkersChannels []chan bool
-	for true {
+	for {
 		// Wait until we've got more work to do.
 		select {
 		case <-ace.Closing:
@@ -201,12 +203,17 @@ func (ace *ACMEChallengeEngine) _run(b *backend, state *acmeState) error {
 			// looping through the queue until we hit a repeat.
 			firstIdentifier = ""
 
+			// If we are no longer the active node, break out
+			if b.System().ReplicationState().HasState(consts.ReplicationDRSecondary | consts.ReplicationPerformanceStandby) {
+				break
+			}
+
 			// Here, we got a piece of work that is ready to check; create a
 			// channel and a new go routine and run it. Note that this still
 			// could have a RetryAfter date we're not aware of (e.g., if the
 			// cluster restarted as we do not read the entries there).
 			channel := make(chan bool, 1)
-			go ace.VerifyChallenge(runnerSC, task.Identifier, channel, config)
+			go ace.VerifyChallenge(runnerSC, task.Identifier, task.NumRetries, channel, config)
 			finishedWorkersChannels = append(finishedWorkersChannels, channel)
 			startedWork = true
 		}
@@ -305,8 +312,9 @@ func (ace *ACMEChallengeEngine) AcceptChallenge(sc *storageContext, account stri
 	return nil
 }
 
-func (ace *ACMEChallengeEngine) VerifyChallenge(runnerSc *storageContext, id string, finished chan bool, config *acmeConfigEntry) {
-	sc, _ /* cancel func */ := runnerSc.WithFreshTimeout(MaxChallengeTimeout)
+func (ace *ACMEChallengeEngine) VerifyChallenge(runnerSc *storageContext, id string, validationQueueRetries int, finished chan bool, config *acmeConfigEntry) {
+	sc, cancel := runnerSc.WithFreshTimeout(MaxChallengeTimeout)
+	defer cancel()
 	runnerSc.Backend.Logger().Debug("Starting verification of challenge", "id", id)
 
 	if retry, retryAfter, err := ace._verifyChallenge(sc, id, config); err != nil {
@@ -316,11 +324,28 @@ func (ace *ACMEChallengeEngine) VerifyChallenge(runnerSc *storageContext, id str
 		sc.Backend.Logger().Error(fmt.Sprintf("ACME validation failed for %v: %v", id, err))
 
 		if retry {
+			validationQueueRetries++
+
+			// The retry logic within _verifyChallenge is dependent on being able to read and decode
+			// the ACME challenge entries. If we encounter such failures we would retry forever, so
+			// we have a secondary check here to see if we are consistently looping within the validation
+			// queue that is larger than the normal retry attempts we would allow.
+			if validationQueueRetries > MaxRetryAttempts*2 {
+				sc.Backend.Logger().Warn("reached max error attempts within challenge queue: %v, giving up", id)
+				_, _, err = ace._verifyChallengeCleanup(sc, nil, id)
+				if err != nil {
+					sc.Backend.Logger().Warn("Failed cleaning up challenge entry: %v", err)
+				}
+				finished <- true
+				return
+			}
+
 			ace.ValidationLock.Lock()
 			defer ace.ValidationLock.Unlock()
 			ace.Validations.PushBack(&ChallengeQueueEntry{
 				Identifier: id,
 				RetryAfter: retryAfter,
+				NumRetries: validationQueueRetries,
 			})
 
 			// Let the validator know there's a pending challenge.
@@ -343,23 +368,23 @@ func (ace *ACMEChallengeEngine) VerifyChallenge(runnerSc *storageContext, id str
 
 func (ace *ACMEChallengeEngine) _verifyChallenge(sc *storageContext, id string, config *acmeConfigEntry) (bool, time.Time, error) {
 	now := time.Now()
+	backoffTime := now.Add(1 * time.Second)
 	path := acmeValidationPrefix + id
 	challengeEntry, err := sc.Storage.Get(sc.Context, path)
 	if err != nil {
-		return true, now, fmt.Errorf("error loading challenge %v: %w", id, err)
+		return true, backoffTime, fmt.Errorf("error loading challenge %v: %w", id, err)
 	}
 
 	if challengeEntry == nil {
 		// Something must've successfully cleaned up our storage entry from
 		// under us. Assume we don't need to rerun, else the client will
 		// trigger us to re-run.
-		err = nil
-		return ace._verifyChallengeCleanup(sc, err, id)
+		return ace._verifyChallengeCleanup(sc, nil, id)
 	}
 
 	var cv *ChallengeValidation
 	if err := challengeEntry.DecodeJSON(&cv); err != nil {
-		return true, now, fmt.Errorf("error decoding challenge %v: %w", id, err)
+		return true, backoffTime, fmt.Errorf("error decoding challenge %v: %w", id, err)
 	}
 
 	if now.Before(cv.RetryAfter) {
@@ -369,7 +394,7 @@ func (ace *ACMEChallengeEngine) _verifyChallenge(sc *storageContext, id string,
 	authzPath := getAuthorizationPath(cv.Account, cv.Authorization)
 	authz, err := loadAuthorizationAtPath(sc, authzPath)
 	if err != nil {
-		return true, now, fmt.Errorf("error loading authorization %v/%v for challenge %v: %w", cv.Account, cv.Authorization, id, err)
+		return true, backoffTime, fmt.Errorf("error loading authorization %v/%v for challenge %v: %w", cv.Account, cv.Authorization, id, err)
 	}
 
 	if authz.Status != ACMEAuthorizationPending {
@@ -527,7 +552,7 @@ func (ace *ACMEChallengeEngine) _verifyChallengeCleanup(sc *storageContext, err
 
 	// Remove our ChallengeValidation entry only.
 	if deleteErr := sc.Storage.Delete(sc.Context, acmeValidationPrefix+id); deleteErr != nil {
-		return true, now.Add(-1 * time.Second), fmt.Errorf("error deleting challenge %v (error prior to cleanup, if any: %v): %w", id, err, deleteErr)
+		return true, now.Add(1 * time.Second), fmt.Errorf("error deleting challenge %v (error prior to cleanup, if any: %v): %w", id, err, deleteErr)
 	}
 
 	if err != nil {
diff --git a/builtin/logical/pki/acme_state.go b/builtin/logical/pki/acme_state.go
index 88c300ab8..d647450e3 100644
--- a/builtin/logical/pki/acme_state.go
+++ b/builtin/logical/pki/acme_state.go
@@ -18,6 +18,7 @@ import (
 
 	"github.com/hashicorp/go-secure-stdlib/nonceutil"
 	"github.com/hashicorp/vault/sdk/framework"
+	"github.com/hashicorp/vault/sdk/helper/consts"
 	"github.com/hashicorp/vault/sdk/logical"
 )
 
@@ -76,6 +77,13 @@ func (a *acmeState) Initialize(b *backend, sc *storageContext) error {
 		return fmt.Errorf("error initializing ACME engine: %w", err)
 	}
 
+	if b.System().ReplicationState().HasState(consts.ReplicationDRSecondary | consts.ReplicationPerformanceStandby) {
+		// It is assumed, that if the node does become the active node later
+		// the plugin is re-initialized, so this is safe. It also spares the node
+		// from loading the existing queue into memory for no reason.
+		b.Logger().Debug("Not on an active node, skipping starting ACME challenge validation engine")
+		return nil
+	}
 	// Kick off our ACME challenge validation engine.
 	go a.validator.Run(b, a, sc)
 
diff --git a/builtin/logical/pki/dnstest/server.go b/builtin/logical/pki/dnstest/server.go
index b0b6d1a36..4b7189c32 100644
--- a/builtin/logical/pki/dnstest/server.go
+++ b/builtin/logical/pki/dnstest/server.go
@@ -64,9 +64,10 @@ func (ts *TestServer) setupRunner(domain string, network string) {
 		ContainerName: "bind9-dns-" + strings.ReplaceAll(domain, ".", "-"),
 		NetworkName:   network,
 		Ports:         []string{"53/udp"},
-		LogConsumer: func(s string) {
-			ts.log.Info(s)
-		},
+		// DNS container logging was disabled to reduce content within CI logs.
+		//LogConsumer: func(s string) {
+		//	ts.log.Info(s)
+		//},
 	})
 	require.NoError(ts.t, err)
 }
diff --git a/changelog/23278.txt b/changelog/23278.txt
new file mode 100644
index 000000000..cd02679e7
--- /dev/null
+++ b/changelog/23278.txt
@@ -0,0 +1,3 @@
+```release-note:bug
+secrets/pki: Stop processing in-flight ACME verifications when an active node steps down
+```