diff --git a/changelog/15204.txt b/changelog/15204.txt
new file mode 100644
index 000000000..f4c5b8cc4
--- /dev/null
+++ b/changelog/15204.txt
@@ -0,0 +1,3 @@
+```release-note:improvement
+agent/auto-auth: Add `min_backoff` to the method stanza for configuring initial backoff duration.
+```
diff --git a/command/agent.go b/command/agent.go
index 6bafd4cb0..2b8486515 100644
--- a/command/agent.go
+++ b/command/agent.go
@@ -790,10 +790,19 @@ func (c *AgentCommand) Run(args []string) int {
 	// Start auto-auth and sink servers
 	if method != nil {
 		enableTokenCh := len(config.Templates) > 0
+
+		// Auth Handler is going to set its own retry values, so we want to
+		// work on a copy of the client to not affect other subsystems.
+		clonedClient, err := c.client.Clone()
+		if err != nil {
+			c.UI.Error(fmt.Sprintf("Error cloning client for auth handler: %v", err))
+			return 1
+		}
 		ah := auth.NewAuthHandler(&auth.AuthHandlerConfig{
 			Logger:                       c.logger.Named("auth.handler"),
-			Client:                       c.client,
+			Client:                       clonedClient,
 			WrapTTL:                      config.AutoAuth.Method.WrapTTL,
+			MinBackoff:                   config.AutoAuth.Method.MinBackoff,
 			MaxBackoff:                   config.AutoAuth.Method.MaxBackoff,
 			EnableReauthOnNewCredentials: config.AutoAuth.EnableReauthOnNewCredentials,
 			EnableTemplateTokenCh:        enableTokenCh,
diff --git a/command/agent/auth/auth.go b/command/agent/auth/auth.go
index c00028608..7406d7c8c 100644
--- a/command/agent/auth/auth.go
+++ b/command/agent/auth/auth.go
@@ -15,7 +15,7 @@ import (
 )
 
 const (
-	initialBackoff    = 1 * time.Second
+	defaultMinBackoff = 1 * time.Second
 	defaultMaxBackoff = 5 * time.Minute
 )
 
@@ -55,6 +55,7 @@ type AuthHandler struct {
 	random                       *rand.Rand
 	wrapTTL                      time.Duration
 	maxBackoff                   time.Duration
+	minBackoff                   time.Duration
 	enableReauthOnNewCredentials bool
 	enableTemplateTokenCh        bool
 }
@@ -64,6 +65,7 @@ type AuthHandlerConfig struct {
 	Client                       *api.Client
 	WrapTTL                      time.Duration
 	MaxBackoff                   time.Duration
+	MinBackoff                   time.Duration
 	Token                        string
 	EnableReauthOnNewCredentials bool
 	EnableTemplateTokenCh        bool
@@ -80,6 +82,7 @@ func NewAuthHandler(conf *AuthHandlerConfig) *AuthHandler {
 		client:                       conf.Client,
 		random:                       rand.New(rand.NewSource(int64(time.Now().Nanosecond()))),
 		wrapTTL:                      conf.WrapTTL,
+		minBackoff:                   conf.MinBackoff,
 		maxBackoff:                   conf.MaxBackoff,
 		enableReauthOnNewCredentials: conf.EnableReauthOnNewCredentials,
 		enableTemplateTokenCh:        conf.EnableTemplateTokenCh,
@@ -104,7 +107,15 @@ func (ah *AuthHandler) Run(ctx context.Context, am AuthMethod) error {
 		return errors.New("auth handler: nil auth method")
 	}
 
-	backoff := newAgentBackoff(ah.maxBackoff)
+	if ah.minBackoff <= 0 {
+		ah.minBackoff = defaultMinBackoff
+	}
+
+	backoff := newAgentBackoff(ah.minBackoff, ah.maxBackoff)
+
+	if backoff.min >= backoff.max {
+		return errors.New("auth handler: min_backoff cannot be greater than max_backoff")
+	}
 
 	ah.logger.Info("starting auth handler")
 	defer func() {
@@ -164,6 +175,10 @@ func (ah *AuthHandler) Run(ctx context.Context, am AuthMethod) error {
 			clientToUse = ah.client
 		}
 
+		// Disable retry on the client to ensure our backoffOrQuit function is
+		// the only source of retry/backoff.
+		clientToUse.SetMaxRetries(0)
+
 		var secret *api.Secret = new(api.Secret)
 		if first && ah.token != "" {
 			ah.logger.Debug("using preloaded token")
@@ -342,18 +357,24 @@ func (ah *AuthHandler) Run(ctx context.Context, am AuthMethod) error {
 
 // agentBackoff tracks exponential backoff state.
 type agentBackoff struct {
+	min     time.Duration
 	max     time.Duration
 	current time.Duration
 }
 
-func newAgentBackoff(max time.Duration) *agentBackoff {
+func newAgentBackoff(min, max time.Duration) *agentBackoff {
 	if max <= 0 {
 		max = defaultMaxBackoff
 	}
 
+	if min <= 0 {
+		min = defaultMinBackoff
+	}
+
 	return &agentBackoff{
+		current: min,
 		max:     max,
-		current: initialBackoff,
+		min:     min,
 	}
 }
 
@@ -372,7 +393,7 @@ func (b *agentBackoff) next() {
 }
 
 func (b *agentBackoff) reset() {
-	b.current = initialBackoff
+	b.current = b.min
 }
 
 func (b agentBackoff) String() string {
diff --git a/command/agent/auth/auth_test.go b/command/agent/auth/auth_test.go
index 05c24fe1f..e0c2442d3 100644
--- a/command/agent/auth/auth_test.go
+++ b/command/agent/auth/auth_test.go
@@ -109,10 +109,10 @@ consumption:
 
 func TestAgentBackoff(t *testing.T) {
 	max := 1024 * time.Second
-	backoff := newAgentBackoff(max)
+	backoff := newAgentBackoff(defaultMinBackoff, max)
 
 	// Test initial value
-	if backoff.current != initialBackoff {
+	if backoff.current != defaultMinBackoff {
 		t.Fatalf("expected 1s initial backoff, got: %v", backoff.current)
 	}
 
@@ -139,7 +139,58 @@ func TestAgentBackoff(t *testing.T) {
 
 	// Test reset
 	backoff.reset()
-	if backoff.current != initialBackoff {
+	if backoff.current != defaultMinBackoff {
 		t.Fatalf("expected 1s backoff after reset, got: %v", backoff.current)
 	}
 }
+
+func TestAgentMinBackoffCustom(t *testing.T) {
+	type test struct {
+		minBackoff time.Duration
+		want       time.Duration
+	}
+
+	tests := []test{
+		{minBackoff: 0 * time.Second, want: 1 * time.Second},
+		{minBackoff: 1 * time.Second, want: 1 * time.Second},
+		{minBackoff: 5 * time.Second, want: 5 * time.Second},
+		{minBackoff: 10 * time.Second, want: 10 * time.Second},
+	}
+
+	for _, test := range tests {
+		max := 1024 * time.Second
+		backoff := newAgentBackoff(test.minBackoff, max)
+
+		// Test initial value
+		if backoff.current != test.want {
+			t.Fatalf("expected %d initial backoff, got: %v", test.want, backoff.current)
+		}
+
+		// Test that backoff values are in expected range (75-100% of 2*previous)
+		for i := 0; i < 5; i++ {
+			old := backoff.current
+			backoff.next()
+
+			expMax := 2 * old
+			expMin := 3 * expMax / 4
+
+			if backoff.current < expMin || backoff.current > expMax {
+				t.Fatalf("expected backoff in range %v to %v, got: %v", expMin, expMax, backoff)
+			}
+		}
+
+		// Test that backoff is capped
+		for i := 0; i < 100; i++ {
+			backoff.next()
+			if backoff.current > max {
+				t.Fatalf("backoff exceeded max of 100s: %v", backoff)
+			}
+		}
+
+		// Test reset
+		backoff.reset()
+		if backoff.current != test.want {
+			t.Fatalf("expected %d backoff after reset, got: %v", test.want, backoff.current)
+		}
+	}
+}
diff --git a/command/agent/config/config.go b/command/agent/config/config.go
index 7a105573d..e68af26f6 100644
--- a/command/agent/config/config.go
+++ b/command/agent/config/config.go
@@ -112,6 +112,8 @@ type Method struct {
 	MountPath     string        `hcl:"mount_path"`
 	WrapTTLRaw    interface{}   `hcl:"wrap_ttl"`
 	WrapTTL       time.Duration `hcl:"-"`
+	MinBackoffRaw interface{}   `hcl:"min_backoff"`
+	MinBackoff    time.Duration `hcl:"-"`
 	MaxBackoffRaw interface{}   `hcl:"max_backoff"`
 	MaxBackoff    time.Duration `hcl:"-"`
 	Namespace     string        `hcl:"namespace"`
@@ -470,6 +472,14 @@ func parseAutoAuth(result *Config, list *ast.ObjectList) error {
 		result.AutoAuth.Method.MaxBackoffRaw = nil
 	}
 
+	if result.AutoAuth.Method.MinBackoffRaw != nil {
+		var err error
+		if result.AutoAuth.Method.MinBackoff, err = parseutil.ParseDurationSecond(result.AutoAuth.Method.MinBackoffRaw); err != nil {
+			return err
+		}
+		result.AutoAuth.Method.MinBackoffRaw = nil
+	}
+
 	return nil
 }
 
diff --git a/command/agent/config/config_test.go b/command/agent/config/config_test.go
index 2bb8844ba..1a1aec2a1 100644
--- a/command/agent/config/config_test.go
+++ b/command/agent/config/config_test.go
@@ -290,6 +290,49 @@ func TestLoadConfigFile_Method_Wrapping(t *testing.T) {
 	}
 }
 
+func TestLoadConfigFile_Method_InitialBackoff(t *testing.T) {
+	config, err := LoadConfig("./test-fixtures/config-method-initial-backoff.hcl")
+	if err != nil {
+		t.Fatalf("err: %s", err)
+	}
+
+	expected := &Config{
+		SharedConfig: &configutil.SharedConfig{
+			PidFile: "./pidfile",
+		},
+		AutoAuth: &AutoAuth{
+			Method: &Method{
+				Type:       "aws",
+				MountPath:  "auth/aws",
+				WrapTTL:    5 * time.Minute,
+				MinBackoff: 5 * time.Second,
+				MaxBackoff: 2 * time.Minute,
+				Config: map[string]interface{}{
+					"role": "foobar",
+				},
+			},
+			Sinks: []*Sink{
+				{
+					Type: "file",
+					Config: map[string]interface{}{
+						"path": "/tmp/file-foo",
+					},
+				},
+			},
+		},
+		Vault: &Vault{
+			Retry: &Retry{
+				NumRetries: 12,
+			},
+		},
+	}
+
+	config.Prune()
+	if diff := deep.Equal(config, expected); diff != nil {
+		t.Fatal(diff)
+	}
+}
+
 func TestLoadConfigFile_AgentCache_NoAutoAuth(t *testing.T) {
 	config, err := LoadConfig("./test-fixtures/config-cache-no-auto_auth.hcl")
 	if err != nil {
diff --git a/command/agent/config/test-fixtures/config-method-initial-backoff.hcl b/command/agent/config/test-fixtures/config-method-initial-backoff.hcl
new file mode 100644
index 000000000..6b9343aa4
--- /dev/null
+++ b/command/agent/config/test-fixtures/config-method-initial-backoff.hcl
@@ -0,0 +1,20 @@
+pid_file = "./pidfile"
+
+auto_auth {
+	method {
+		type = "aws"
+		wrap_ttl = 300
+		config = {
+			role = "foobar"
+		}
+		max_backoff = "2m"
+        min_backoff = "5s"
+	}
+
+	sink {
+		type = "file"
+		config = {
+			path = "/tmp/file-foo"
+		}
+	}
+}
diff --git a/command/agent/template/template.go b/command/agent/template/template.go
index cf21944ab..9ff22fbd9 100644
--- a/command/agent/template/template.go
+++ b/command/agent/template/template.go
@@ -311,6 +311,19 @@ func newRunnerConfig(sc *ServerConfig, templates ctconfig.TemplateConfigs) (*ctc
 		Enabled:  &enabled,
 	}
 
+	// Sync Consul Template's retry with user set auto-auth initial backoff value.
+	// This is helpful if Auto Auth cannot get a new token and CT is trying to fetch
+	// secrets.
+	if sc.AgentConfig.AutoAuth != nil && sc.AgentConfig.AutoAuth.Method != nil {
+		if sc.AgentConfig.AutoAuth.Method.MinBackoff > 0 {
+			conf.Vault.Retry.Backoff = &sc.AgentConfig.AutoAuth.Method.MinBackoff
+		}
+
+		if sc.AgentConfig.AutoAuth.Method.MaxBackoff > 0 {
+			conf.Vault.Retry.MaxBackoff = &sc.AgentConfig.AutoAuth.Method.MaxBackoff
+		}
+	}
+
 	conf.Finalize()
 
 	// setup log level from TemplateServer config
diff --git a/website/content/docs/agent/autoauth/index.mdx b/website/content/docs/agent/autoauth/index.mdx
index 5a87359c8..922c7427e 100644
--- a/website/content/docs/agent/autoauth/index.mdx
+++ b/website/content/docs/agent/autoauth/index.mdx
@@ -138,9 +138,17 @@ These are common configuration values that live within the `method` block:
   structure. Values can be an integer number of seconds or a stringish value
   like `5m`.
 
+- `min_backoff` `(string or integer: "1s")` - The minimum backoff time Agent 
+  will delay before retrying after a failed auth attempt. The backoff will start 
+  at the configured value and double (with some randomness) after successive 
+  failures, capped by `max_backoff.` If Agent templating is being used, this 
+  value is also used as the min backoff time for the templating server.
+
 - `max_backoff` `(string or integer: "5m")` - The maximum time Agent will delay
-  before retrying after a failed auth attempt. The backoff will start at 1 second
+  before retrying after a failed auth attempt. The backoff will start at `min_backoff` 
   and double (with some randomness) after successive failures, capped by `max_backoff.`
+  If Agent templating is being used, this value is also used as the max backoff time 
+  for the templating server.
 
 - `config` `(object: required)` - Configuration of the method itself. See the
   sidebar for information about each method.