diff --git a/operator/internal/webhook/injector/container_builder.go b/operator/internal/webhook/injector/container_builder.go
index 62d17b0a..3e09bf61 100644
--- a/operator/internal/webhook/injector/container_builder.go
+++ b/operator/internal/webhook/injector/container_builder.go
@@ -100,7 +100,7 @@ func (b *ContainerBuilder) BuildEnvoyProxyContainerWithSpireOption(spireEnabled
 		},
 		{
 			Name:      "authproxy-routes",
-			MountPath: "/etc/authproxy",
+			MountPath: AuthProxyMountPath,
 			ReadOnly:  true,
 		},
 		{
@@ -266,7 +266,7 @@ func (b *ContainerBuilder) buildProxySidecarContainer(spireEnabled bool, image,
 		},
 		{
 			Name:      AuthproxyRoutesConfigMapName,
-			MountPath: "/etc/authproxy",
+			MountPath: AuthProxyMountPath,
 			ReadOnly:  true,
 		},
 	}
@@ -345,7 +345,7 @@ func (b *ContainerBuilder) buildEnvoyProxyEnvResolved() []corev1.EnvVar {
 		{Name: "TARGET_SCOPES", Value: b.resolved.TargetScopes},
 		{Name: "CLIENT_ID_FILE", Value: "/shared/client-id.txt"},
 		{Name: "CLIENT_SECRET_FILE", Value: "/shared/client-secret.txt"},
-		{Name: "ROUTES_CONFIG_PATH", Value: "/etc/authproxy/routes.yaml"},
+		{Name: "ROUTES_CONFIG_PATH", Value: AuthProxyRoutesFile},
 		{Name: "DEFAULT_OUTBOUND_POLICY", Value: b.resolved.DefaultOutboundPolicy},
 	}
 }
@@ -433,7 +433,7 @@ func (b *ContainerBuilder) buildEnvoyProxyEnvLegacy() []corev1.EnvVar {
 		},
 		{
 			Name:  "ROUTES_CONFIG_PATH",
-			Value: "/etc/authproxy/routes.yaml",
+			Value: AuthProxyRoutesFile,
 		},
 		{
 			Name: "DEFAULT_OUTBOUND_POLICY",
diff --git a/operator/internal/webhook/injector/namespace_config.go b/operator/internal/webhook/injector/namespace_config.go
index 00d81332..0218e8fd 100644
--- a/operator/internal/webhook/injector/namespace_config.go
+++ b/operator/internal/webhook/injector/namespace_config.go
@@ -37,6 +37,12 @@ const (
 	AuthproxyRoutesConfigMapName   = "authproxy-routes"
 )
 
+// AuthBridge sidecar container paths.
+const (
+	AuthProxyMountPath  = "/etc/authproxy"
+	AuthProxyRoutesFile = AuthProxyMountPath + "/routes.yaml"
+)
+
 // NamespaceConfig holds resolved values from namespace ConfigMaps/Secrets.
 type NamespaceConfig struct {
 	// From "authbridge-config" ConfigMap
diff --git a/operator/internal/webhook/injector/pod_mutator.go b/operator/internal/webhook/injector/pod_mutator.go
index 7a41df5b..16152c1d 100644
--- a/operator/internal/webhook/injector/pod_mutator.go
+++ b/operator/internal/webhook/injector/pod_mutator.go
@@ -773,7 +773,7 @@ func (m *PodMutator) InjectAuthBridge(ctx context.Context, podSpec *corev1.PodSp
 			listenerOverrides["reverse_proxy_addr"] = fmt.Sprintf(":%d", originalAgentPort)
 			listenerOverrides["reverse_proxy_backend"] = fmt.Sprintf("http://127.0.0.1:%d", newAgentPort)
 		}
-		perAgentCMName, err := m.ensurePerAgentConfigMap(ctx, namespace, crName,
+		perAgentCMName, routesCMName, err := m.ensurePerAgentConfigMap(ctx, namespace, crName,
 			ModeProxySidecar, nsConfig.AuthBridgeRuntimeYAML, nsConfig,
 			listenerOverrides,
 			mtlsMode, tlsBridgeMode, spireEnabled, agentRuntime)
@@ -875,6 +875,12 @@ func (m *PodMutator) InjectAuthBridge(ctx context.Context, podSpec *corev1.PodSp
 		// requiredVolumes is always set above (resolved or legacy path) before
 		// the mode switch, so it is never nil here.
 		proxyVolumes := overrideAuthBridgeConfigMapInVolumes(requiredVolumes, perAgentCMName)
+
+		// Override authproxy-routes volume if routes ConfigMap was created
+		if routesCMName != "" {
+			proxyVolumes = overrideRoutesConfigMapInVolumes(proxyVolumes, routesCMName)
+		}
+
 		for i := range proxyVolumes {
 			if !volumeExists(podSpec.Volumes, proxyVolumes[i].Name) {
 				podSpec.Volumes = append(podSpec.Volumes, proxyVolumes[i])
@@ -945,13 +951,18 @@ func (m *PodMutator) InjectAuthBridge(ctx context.Context, podSpec *corev1.PodSp
 	// data plane terminates the actual TLS — DownstreamTlsContext on the
 	// inbound listener (gated on MTLSEnabled) and UpstreamTlsContext on
 	// original_destination_tls (strict only).
-	perAgentCMName, err := m.ensurePerAgentConfigMap(ctx, namespace, crName,
+	perAgentCMName, routesCMName, err := m.ensurePerAgentConfigMap(ctx, namespace, crName,
 		ModeEnvoySidecar, nsConfig.AuthBridgeRuntimeYAML, nsConfig, nil, mtlsMode, "", spireEnabled, agentRuntime) // bridge never runs under envoy-sidecar
 	if err != nil {
 		return false, fmt.Errorf("envoy-sidecar per-agent ConfigMap: %w", err)
 	}
 	requiredVolumes = overrideAuthBridgeConfigMapInVolumes(requiredVolumes, perAgentCMName)
 
+	// Override authproxy-routes volume if routes ConfigMap was created
+	if routesCMName != "" {
+		requiredVolumes = overrideRoutesConfigMapInVolumes(requiredVolumes, routesCMName)
+	}
+
 	resolvedForEnvoy := ResolveConfig(currentConfig, nsConfig)
 	resolvedForEnvoy.MTLSMode = mtlsMode
 	envoyCMName, err := m.ensurePerAgentEnvoyConfigMap(ctx, namespace, crName, resolvedForEnvoy)
@@ -1174,7 +1185,7 @@ func (m *PodMutator) ensurePerAgentConfigMap(
 	tlsBridgeMode string,
 	spireEnabled bool,
 	agentRuntime *agentv1alpha1.AgentRuntime,
-) (string, error) {
+) (configCMName string, routesCMName string, err error) {
 	cmName := perAgentConfigMapName(crName)
 
 	// Parse the base YAML into a generic map
@@ -1263,10 +1274,14 @@ func (m *PodMutator) ensurePerAgentConfigMap(
 	// Routes tell AuthBridge which audiences to request when calling specific
 	// destinations. Routes are only effective when the namespace is configured
 	// with SPIFFE authentication (CLIENT_AUTH_TYPE=federated-jwt).
+	//
+	// Routes are written to a separate ConfigMap and mounted at /etc/authproxy/routes.yaml.
+	// The config.yaml references the file path rather than containing routes inline.
+	var routesData []byte
 	if agentRuntime != nil && agentRuntime.Spec.Auth != nil &&
 		len(agentRuntime.Spec.Auth.Outbound) > 0 {
 
-		// Navigate to pipeline.outbound.plugins[token-exchange].config
+		// Configure token-exchange plugin to read routes from file
 		pipeline, _ := cfg["pipeline"].(map[string]interface{})
 		if pipeline == nil {
 			mutatorLog.Info("WARN: no pipeline block found, cannot inject routes",
@@ -1282,7 +1297,7 @@ func (m *PodMutator) ensurePerAgentConfigMap(
 					mutatorLog.Info("WARN: no outbound plugins found, cannot inject routes",
 						"namespace", namespace, "crName", crName)
 				} else {
-					// Find the token-exchange plugin
+					// Find the token-exchange plugin and configure it to read routes from file
 					for i := range plugins {
 						plugin, _ := plugins[i].(map[string]interface{})
 						if plugin == nil {
@@ -1296,41 +1311,71 @@ func (m *PodMutator) ensurePerAgentConfigMap(
 								plugin["config"] = pluginConfig
 							}
 
-							// Generate routes from spec.auth.outbound
-							routes := make([]interface{}, 0, len(agentRuntime.Spec.Auth.Outbound))
-							for _, outboundRoute := range agentRuntime.Spec.Auth.Outbound {
-								route := map[string]interface{}{
-									"audiences": outboundRoute.Audiences,
-								}
-
-								// Add destination match (host or hostRegex)
-								destination := make(map[string]interface{})
-								if outboundRoute.Destination.Host != "" {
-									destination["host"] = outboundRoute.Destination.Host
-								}
-								if outboundRoute.Destination.HostRegex != "" {
-									destination["hostRegex"] = outboundRoute.Destination.HostRegex
-								}
-								route["destination"] = destination
-
-								routes = append(routes, route)
+							// Set routes to reference external file
+							pluginConfig["routes"] = map[string]interface{}{
+								"file": AuthProxyRoutesFile,
 							}
 
-							pluginConfig["routes"] = routes
-							mutatorLog.Info("injected token-exchange routes from AgentRuntime spec.auth",
-								"namespace", namespace, "crName", crName, "routeCount", len(routes))
+							mutatorLog.Info("configured token-exchange to read routes from file",
+								"namespace", namespace, "crName", crName, "routeCount", len(agentRuntime.Spec.Auth.Outbound))
 							break
 						}
 					}
 				}
 			}
 		}
+
+		// Generate routes.yaml content in AuthBridge's routing.Route format:
+		// - host: "hostname"  (flat, not nested under destination)
+		// - target_audience: "audience"  (single string, not audiences array)
+		routes := make([]interface{}, 0, len(agentRuntime.Spec.Auth.Outbound))
+		for _, outboundRoute := range agentRuntime.Spec.Auth.Outbound {
+			route := make(map[string]interface{})
+
+			// Host or HostRegex (flat fields, not nested)
+			if outboundRoute.Destination.Host != "" {
+				route["host"] = outboundRoute.Destination.Host
+			}
+			if outboundRoute.Destination.HostRegex != "" {
+				// AuthBridge router uses glob patterns, not regex. The CRD field name
+				// "hostRegex" is misleading - it should contain glob syntax (*.example.com),
+				// not regex syntax (.*\.example\.com). Warn users about this.
+				mutatorLog.Info("hostRegex field is mapped to AuthBridge glob pattern (not regex)",
+					"namespace", namespace, "crName", crName,
+					"hostRegex", outboundRoute.Destination.HostRegex,
+					"note", "use glob syntax like '*.team1.svc.cluster.local', not regex '.*\\.team1\\.svc\\.cluster\\.local'")
+				route["host"] = outboundRoute.Destination.HostRegex
+			}
+
+			// target_audience is a single string, not array
+			// Take first audience if multiple specified
+			if len(outboundRoute.Audiences) > 0 {
+				route["target_audience"] = outboundRoute.Audiences[0]
+
+				// Warn if multiple audiences specified (only first is used)
+				// See https://github.com/rossoctl/operator/issues/518
+				if len(outboundRoute.Audiences) > 1 {
+					mutatorLog.Info("multiple audiences specified but only first will be used",
+						"namespace", namespace, "crName", crName,
+						"route", outboundRoute.Destination.Host,
+						"audiences", outboundRoute.Audiences,
+						"using", outboundRoute.Audiences[0])
+				}
+			}
+
+			routes = append(routes, route)
+		}
+
+		routesData, err = yaml.Marshal(routes)
+		if err != nil {
+			return "", "", fmt.Errorf("failed to marshal routes for %s/%s: %w", namespace, crName, err)
+		}
 	}
 
 	// Marshal back to YAML
 	data, err := yaml.Marshal(cfg)
 	if err != nil {
-		return "", fmt.Errorf("failed to marshal per-agent config for %s/%s: %w", namespace, crName, err)
+		return "", "", fmt.Errorf("failed to marshal per-agent config for %s/%s: %w", namespace, crName, err)
 	}
 
 	// Server-side apply: atomic create-or-update in a single API call.
@@ -1346,12 +1391,32 @@ func (m *PodMutator) ensurePerAgentConfigMap(
 	}
 
 	if err := m.Client.Apply(ctx, cmApply, client.FieldOwner("rossoctl-webhook"), client.ForceOwnership); err != nil {
-		return "", fmt.Errorf("failed to apply per-agent ConfigMap %s/%s: %w", namespace, cmName, err)
+		return "", "", fmt.Errorf("failed to apply per-agent ConfigMap %s/%s: %w", namespace, cmName, err)
 	}
 	mutatorLog.Info("Applied per-agent ConfigMap",
 		"namespace", namespace, "name", cmName, "mode", mode, "mtlsMode", mtlsMode)
 
-	return cmName, nil
+	// Create separate routes ConfigMap if routes are present
+	if len(routesData) > 0 {
+		routesCMName := "authbridge-routes-" + crName
+		routesCMApply := applyconfigscorev1.ConfigMap(routesCMName, namespace).
+			WithLabels(map[string]string{managedByLabel: managedByValue}).
+			WithData(map[string]string{"routes.yaml": string(routesData)})
+
+		// Set same OwnerReference for garbage collection
+		if ownerRef := m.buildOwnerReference(ctx, namespace, crName); ownerRef != nil {
+			routesCMApply = routesCMApply.WithOwnerReferences(ownerRef)
+		}
+
+		if err := m.Client.Apply(ctx, routesCMApply, client.FieldOwner("rossoctl-webhook"), client.ForceOwnership); err != nil {
+			return "", "", fmt.Errorf("failed to apply routes ConfigMap %s/%s: %w", namespace, routesCMName, err)
+		}
+		mutatorLog.Info("Applied routes ConfigMap",
+			"namespace", namespace, "name", routesCMName, "routeCount", len(agentRuntime.Spec.Auth.Outbound))
+		return cmName, routesCMName, nil
+	}
+
+	return cmName, "", nil
 }
 
 // ensurePerAgentEnvoyConfigMap renders an envoy.yaml from the
diff --git a/operator/internal/webhook/injector/pod_mutator_auth_test.go b/operator/internal/webhook/injector/pod_mutator_auth_test.go
index eacfb60f..34384385 100644
--- a/operator/internal/webhook/injector/pod_mutator_auth_test.go
+++ b/operator/internal/webhook/injector/pod_mutator_auth_test.go
@@ -126,7 +126,7 @@ pipeline:
 	}
 
 	// Call ensurePerAgentConfigMap with the AgentRuntime
-	cmName, err := m.ensurePerAgentConfigMap(ctx, "team1", "weather-agent",
+	cmName, routesCMName, err := m.ensurePerAgentConfigMap(ctx, "team1", "weather-agent",
 		ModeProxySidecar, baseYAML, nsConfig, nil, "", "", true, agentRuntime)
 	if err != nil {
 		t.Fatalf("unexpected error: %v", err)
@@ -181,9 +181,33 @@ pipeline:
 		t.Fatal("token-exchange plugin not found")
 	}
 
-	routes, ok := tokenExchangeConfig["routes"].([]interface{})
+	// Verify routes is a file reference, not an inline array
+	routesRef, ok := tokenExchangeConfig["routes"].(map[string]interface{})
 	if !ok {
-		t.Fatal("routes not found or not an array")
+		t.Fatal("routes not found or not a map")
+	}
+	if routesRef["file"] != AuthProxyRoutesFile {
+		t.Errorf("routes file mismatch: got %v, want %s", routesRef["file"], AuthProxyRoutesFile)
+	}
+
+	// Fetch the routes ConfigMap
+	if routesCMName == "" {
+		t.Fatal("routesCMName is empty")
+	}
+	routesCM := &corev1.ConfigMap{}
+	if err := fakeClient.Get(ctx, client.ObjectKey{Namespace: "team1", Name: routesCMName}, routesCM); err != nil {
+		t.Fatalf("failed to get routes ConfigMap: %v", err)
+	}
+
+	// Parse routes.yaml
+	routesYAML, ok := routesCM.Data["routes.yaml"]
+	if !ok {
+		t.Fatal("routes ConfigMap missing routes.yaml key")
+	}
+
+	var routes []interface{}
+	if err := yaml.Unmarshal([]byte(routesYAML), &routes); err != nil {
+		t.Fatalf("failed to parse routes.yaml: %v", err)
 	}
 
 	// Verify we have 2 routes
@@ -191,26 +215,22 @@ pipeline:
 		t.Fatalf("expected 2 routes, got %d", len(routes))
 	}
 
-	// Verify first route (exact host match)
+	// Verify first route (exact host match) - now in flat format
 	route1, _ := routes[0].(map[string]interface{})
-	dest1, _ := route1["destination"].(map[string]interface{})
-	if dest1["host"] != "weather-tool-mcp.team1.svc.cluster.local" {
-		t.Errorf("route 1 host mismatch: got %v", dest1["host"])
+	if route1["host"] != "weather-tool-mcp.team1.svc.cluster.local" {
+		t.Errorf("route 1 host mismatch: got %v", route1["host"])
 	}
-	audiences1, _ := route1["audiences"].([]interface{})
-	if len(audiences1) != 1 || audiences1[0] != "spiffe://localtest.me/ns/team1/sa/weather-tool" {
-		t.Errorf("route 1 audiences mismatch: got %v", audiences1)
+	if route1["target_audience"] != "spiffe://localtest.me/ns/team1/sa/weather-tool" {
+		t.Errorf("route 1 target_audience mismatch: got %v", route1["target_audience"])
 	}
 
-	// Verify second route (regex match)
+	// Verify second route (regex match) - now in flat format
 	route2, _ := routes[1].(map[string]interface{})
-	dest2, _ := route2["destination"].(map[string]interface{})
-	if dest2["hostRegex"] != `.*\.team1\.svc\.cluster\.local` {
-		t.Errorf("route 2 hostRegex mismatch: got %v", dest2["hostRegex"])
+	if route2["host"] != `.*\.team1\.svc\.cluster\.local` {
+		t.Errorf("route 2 host mismatch: got %v", route2["host"])
 	}
-	audiences2, _ := route2["audiences"].([]interface{})
-	if len(audiences2) != 1 || audiences2[0] != "spiffe://localtest.me/ns/team1/sa/default" {
-		t.Errorf("route 2 audiences mismatch: got %v", audiences2)
+	if route2["target_audience"] != "spiffe://localtest.me/ns/team1/sa/default" {
+		t.Errorf("route 2 target_audience mismatch: got %v", route2["target_audience"])
 	}
 }
 
@@ -250,7 +270,7 @@ pipeline:
 	nsConfig := &NamespaceConfig{}
 
 	// Call with nil agentRuntime
-	cmName, err := m.ensurePerAgentConfigMap(ctx, "team1", "my-agent",
+	cmName, _, err := m.ensurePerAgentConfigMap(ctx, "team1", "my-agent",
 		ModeProxySidecar, baseYAML, nsConfig, nil, "", "", false, nil)
 	if err != nil {
 		t.Fatalf("unexpected error: %v", err)
diff --git a/operator/internal/webhook/injector/pod_mutator_test.go b/operator/internal/webhook/injector/pod_mutator_test.go
index eee6bd31..357dde77 100644
--- a/operator/internal/webhook/injector/pod_mutator_test.go
+++ b/operator/internal/webhook/injector/pod_mutator_test.go
@@ -1295,7 +1295,7 @@ func TestEnsurePerAgentConfigMap_EmptyBaseYAML_FallbackFromNsConfig(t *testing.T
 		ClientAuthType:        "client-secret",
 	}
 
-	cmName, err := m.ensurePerAgentConfigMap(ctx, "team1", "weather-service",
+	cmName, _, err := m.ensurePerAgentConfigMap(ctx, "team1", "weather-service",
 		ModeProxySidecar, "", nsConfig, nil, "", "", false, nil)
 	if err != nil {
 		t.Fatalf("unexpected error: %v", err)
@@ -1412,7 +1412,7 @@ pipeline:
             type: spiffe
 `
 
-	cmName, err := m.ensurePerAgentConfigMap(ctx, "team1", "my-agent",
+	cmName, _, err := m.ensurePerAgentConfigMap(ctx, "team1", "my-agent",
 		ModeEnvoySidecar, baseYAML, &NamespaceConfig{}, nil, "", "", false, nil)
 	if err != nil {
 		t.Fatalf("unexpected error: %v", err)
@@ -1471,7 +1471,7 @@ pipeline:
 		"forward_proxy_addr":    ":8081",
 	}
 
-	cmName, err := m.ensurePerAgentConfigMap(ctx, "team1", "my-agent",
+	cmName, _, err := m.ensurePerAgentConfigMap(ctx, "team1", "my-agent",
 		ModeProxySidecar, baseYAML, &NamespaceConfig{}, overrides, "", "", false, nil)
 	if err != nil {
 		t.Fatalf("unexpected error: %v", err)
@@ -1507,7 +1507,7 @@ func TestEnsurePerAgentConfigMap_ExistingCM_OwnedByWebhook_Updated(t *testing.T)
 	m := newTestMutator(existingCM)
 	ctx := context.Background()
 
-	_, err := m.ensurePerAgentConfigMap(ctx, "team1", "my-agent",
+	_, _, err := m.ensurePerAgentConfigMap(ctx, "team1", "my-agent",
 		ModeEnvoySidecar, "", &NamespaceConfig{ClientAuthType: "client-secret"}, nil, "", "", false, nil)
 	if err != nil {
 		t.Fatalf("unexpected error: %v", err)
@@ -1535,7 +1535,7 @@ func TestEnsurePerAgentConfigMap_ExistingCM_OverwrittenBySSA(t *testing.T) {
 	m := newTestMutator(existingCM)
 	ctx := context.Background()
 
-	cmName, err := m.ensurePerAgentConfigMap(ctx, "team1", "my-agent",
+	cmName, _, err := m.ensurePerAgentConfigMap(ctx, "team1", "my-agent",
 		ModeEnvoySidecar, "", &NamespaceConfig{ClientAuthType: "client-secret"}, nil, "", "", false, nil)
 	if err != nil {
 		t.Fatalf("unexpected error: %v", err)
@@ -1563,7 +1563,7 @@ func TestEnsurePerAgentConfigMap_OwnerReference_SetFromDeployment(t *testing.T)
 	m := newTestMutator(deploy)
 	ctx := context.Background()
 
-	cmName, err := m.ensurePerAgentConfigMap(ctx, "team1", "weather-service",
+	cmName, _, err := m.ensurePerAgentConfigMap(ctx, "team1", "weather-service",
 		ModeEnvoySidecar, "", &NamespaceConfig{ClientAuthType: "client-secret"}, nil, "", "", false, nil)
 	if err != nil {
 		t.Fatalf("unexpected error: %v", err)
@@ -1590,7 +1590,7 @@ func TestEnsurePerAgentConfigMap_OwnerReference_SetFromStatefulSet(t *testing.T)
 	m := newTestMutator(sts)
 	ctx := context.Background()
 
-	cmName, err := m.ensurePerAgentConfigMap(ctx, "team1", "my-stateful-agent",
+	cmName, _, err := m.ensurePerAgentConfigMap(ctx, "team1", "my-stateful-agent",
 		ModeEnvoySidecar, "", &NamespaceConfig{ClientAuthType: "client-secret"}, nil, "", "", false, nil)
 	if err != nil {
 		t.Fatalf("unexpected error: %v", err)
@@ -1631,7 +1631,7 @@ func TestEnsurePerAgentConfigMap_OwnerReference_SetFromSandbox(t *testing.T) {
 	}
 	ctx := context.Background()
 
-	cmName, err := m.ensurePerAgentConfigMap(ctx, "team1", "my-sandbox-agent",
+	cmName, _, err := m.ensurePerAgentConfigMap(ctx, "team1", "my-sandbox-agent",
 		ModeEnvoySidecar, "", &NamespaceConfig{ClientAuthType: "client-secret"}, nil, "", "", false, nil)
 	if err != nil {
 		t.Fatalf("unexpected error: %v", err)
@@ -1652,7 +1652,7 @@ func TestEnsurePerAgentConfigMap_OwnerReference_NoWorkload_Skipped(t *testing.T)
 	m := newTestMutator()
 	ctx := context.Background()
 
-	cmName, err := m.ensurePerAgentConfigMap(ctx, "team1", "bare-pod-agent",
+	cmName, _, err := m.ensurePerAgentConfigMap(ctx, "team1", "bare-pod-agent",
 		ModeEnvoySidecar, "", &NamespaceConfig{ClientAuthType: "client-secret"}, nil, "", "", false, nil)
 	if err != nil {
 		t.Fatalf("unexpected error: %v", err)
@@ -1675,7 +1675,7 @@ func TestEnsurePerAgentConfigMap_FederatedJWT_MapsToSpiffe(t *testing.T) {
 		ClientAuthType: "federated-jwt",
 	}
 
-	cmName, err := m.ensurePerAgentConfigMap(ctx, "team1", "spiffe-agent",
+	cmName, _, err := m.ensurePerAgentConfigMap(ctx, "team1", "spiffe-agent",
 		ModeEnvoySidecar, "", nsConfig, nil, "", "", false, nil)
 	if err != nil {
 		t.Fatalf("unexpected error: %v", err)
@@ -1712,7 +1712,7 @@ func TestEnsurePerAgentConfigMap_FederatedJWT_SetsJWTAudience(t *testing.T) {
 		JWTAudience:    "http://keycloak:8080/realms/rossoctl",
 	}
 
-	cmName, err := m.ensurePerAgentConfigMap(ctx, "team1", "spiffe-agent",
+	cmName, _, err := m.ensurePerAgentConfigMap(ctx, "team1", "spiffe-agent",
 		ModeEnvoySidecar, "", nsConfig, nil, "", "", false, nil)
 	if err != nil {
 		t.Fatalf("unexpected error: %v", err)
@@ -1735,7 +1735,7 @@ func TestEnsurePerAgentConfigMap_SpireEnabled_InjectsSpiffeBlock(t *testing.T) {
 	m := newTestMutator()
 	ctx := context.Background()
 
-	cmName, err := m.ensurePerAgentConfigMap(ctx, "team1", "spiffe-agent",
+	cmName, _, err := m.ensurePerAgentConfigMap(ctx, "team1", "spiffe-agent",
 		ModeProxySidecar, "", &NamespaceConfig{}, nil, "", "", true, nil)
 	if err != nil {
 		t.Fatalf("unexpected error: %v", err)
@@ -1757,7 +1757,7 @@ func TestEnsurePerAgentConfigMap_SpireDisabled_NoSpiffeBlock(t *testing.T) {
 	m := newTestMutator()
 	ctx := context.Background()
 
-	cmName, err := m.ensurePerAgentConfigMap(ctx, "team1", "no-spiffe-agent",
+	cmName, _, err := m.ensurePerAgentConfigMap(ctx, "team1", "no-spiffe-agent",
 		ModeProxySidecar, "", &NamespaceConfig{}, nil, "", "", false, nil)
 	if err != nil {
 		t.Fatalf("unexpected error: %v", err)
@@ -1788,7 +1788,7 @@ func TestEnsurePerAgentConfigMap_MTLSStrict_RendersBlock(t *testing.T) {
 	m := newTestMutator()
 	ctx := context.Background()
 
-	cmName, err := m.ensurePerAgentConfigMap(ctx, "team1", "mtls-agent",
+	cmName, _, err := m.ensurePerAgentConfigMap(ctx, "team1", "mtls-agent",
 		ModeProxySidecar, "", &NamespaceConfig{ClientAuthType: "client-secret"}, nil, MTLSModeStrict, "", false, nil)
 	if err != nil {
 		t.Fatalf("unexpected error: %v", err)
@@ -1819,7 +1819,7 @@ func TestEnsurePerAgentConfigMap_MTLSPermissive_RendersBlock(t *testing.T) {
 	m := newTestMutator()
 	ctx := context.Background()
 
-	cmName, err := m.ensurePerAgentConfigMap(ctx, "team1", "mtls-agent",
+	cmName, _, err := m.ensurePerAgentConfigMap(ctx, "team1", "mtls-agent",
 		ModeProxySidecar, "", &NamespaceConfig{ClientAuthType: "client-secret"}, nil, MTLSModePermissive, "", false, nil)
 	if err != nil {
 		t.Fatalf("unexpected error: %v", err)
@@ -1854,7 +1854,7 @@ func TestEnsurePerAgentConfigMap_MTLSDisabled_OmitsBlock(t *testing.T) {
 			m := newTestMutator()
 			ctx := context.Background()
 
-			cmName, err := m.ensurePerAgentConfigMap(ctx, "team1", "no-mtls-"+tt.name,
+			cmName, _, err := m.ensurePerAgentConfigMap(ctx, "team1", "no-mtls-"+tt.name,
 				ModeProxySidecar, "", &NamespaceConfig{ClientAuthType: "client-secret"}, nil, tt.mtlsMode, "", false, nil)
 			if err != nil {
 				t.Fatalf("unexpected error: %v", err)
@@ -1882,7 +1882,7 @@ func TestEnsurePerAgentConfigMap_MTLSScrubsStaleBlock(t *testing.T) {
 	// ConfigMap that was rendered earlier with mtls on.
 	baseYAML := "mode: proxy-sidecar\nmtls:\n  mode: strict\n"
 
-	cmName, err := m.ensurePerAgentConfigMap(ctx, "team1", "scrub-agent",
+	cmName, _, err := m.ensurePerAgentConfigMap(ctx, "team1", "scrub-agent",
 		ModeProxySidecar, baseYAML, &NamespaceConfig{ClientAuthType: "client-secret"}, nil, MTLSModeDisabled, "", false, nil)
 	if err != nil {
 		t.Fatalf("unexpected error: %v", err)
@@ -2103,7 +2103,7 @@ func TestEnsurePerAgentConfigMap_TLSBridgeBlock(t *testing.T) {
 	ctx := context.Background()
 
 	// enabled => tls_bridge: {mode: enabled, ca_dir: <mount>}
-	cmName, err := m.ensurePerAgentConfigMap(ctx, "team1", "bridge-agent",
+	cmName, _, err := m.ensurePerAgentConfigMap(ctx, "team1", "bridge-agent",
 		ModeProxySidecar, "", &NamespaceConfig{}, nil, "", "enabled", false, nil)
 	if err != nil {
 		t.Fatalf("unexpected error: %v", err)
@@ -2121,7 +2121,7 @@ func TestEnsurePerAgentConfigMap_TLSBridgeBlock(t *testing.T) {
 	}
 
 	// disabled ("") => no tls_bridge block
-	cmName2, err := m.ensurePerAgentConfigMap(ctx, "team1", "no-bridge",
+	cmName2, _, err := m.ensurePerAgentConfigMap(ctx, "team1", "no-bridge",
 		ModeProxySidecar, "", &NamespaceConfig{}, nil, "", "", false, nil)
 	if err != nil {
 		t.Fatalf("unexpected error: %v", err)
diff --git a/operator/internal/webhook/injector/volume_builder.go b/operator/internal/webhook/injector/volume_builder.go
index c69fdaaa..cf0e581a 100644
--- a/operator/internal/webhook/injector/volume_builder.go
+++ b/operator/internal/webhook/injector/volume_builder.go
@@ -355,6 +355,24 @@ func overrideAuthBridgeConfigMapInVolumes(volumes []corev1.Volume, cmName string
 	return result
 }
 
+// overrideRoutesConfigMapInVolumes returns a copy of the volume list with
+// the authproxy-routes volume pointing at the given ConfigMap name. Used when
+// AgentRuntime has spec.auth.outbound configured: the per-agent routes live
+// in authbridge-routes-<crName>, replacing the namespace-level "authproxy-routes".
+func overrideRoutesConfigMapInVolumes(volumes []corev1.Volume, routesCMName string) []corev1.Volume {
+	result := make([]corev1.Volume, len(volumes))
+	copy(result, volumes)
+	for i := range result {
+		if result[i].Name == AuthproxyRoutesConfigMapName && result[i].ConfigMap != nil {
+			cmCopy := *result[i].ConfigMap
+			cmCopy.Name = routesCMName
+			cmCopy.Optional = ptr.To(false) // Routes are required when specified
+			result[i].ConfigMap = &cmCopy
+		}
+	}
+	return result
+}
+
 // overrideEnvoyConfigMapInVolumes returns a copy of the volume list with
 // the envoy-config volume pointing at the given ConfigMap name. Used by
 // the envoy-sidecar mTLS path: the rendered per-agent envoy.yaml lives
diff --git a/operator/internal/webhook/injector/volume_builder_test.go b/operator/internal/webhook/injector/volume_builder_test.go
index af34e54f..14608da3 100644
--- a/operator/internal/webhook/injector/volume_builder_test.go
+++ b/operator/internal/webhook/injector/volume_builder_test.go
@@ -35,7 +35,7 @@ func TestBuildResolvedVolumes_SpireDisabled(t *testing.T) {
 		names[v.Name] = true
 	}
 
-	for _, expected := range []string{"shared-data", "envoy-config", "authproxy-routes", "authbridge-runtime-config"} {
+	for _, expected := range []string{"shared-data", "envoy-config", AuthproxyRoutesConfigMapName, "authbridge-runtime-config"} {
 		if !names[expected] {
 			t.Errorf("missing volume %q", expected)
 		}
@@ -62,7 +62,7 @@ func TestBuildResolvedVolumes_SpireEnabled(t *testing.T) {
 		names[v.Name] = true
 	}
 
-	for _, expected := range []string{"shared-data", "spire-agent-socket", "spiffe-helper-config", "svid-output", "envoy-config", "authproxy-routes", "authbridge-runtime-config"} {
+	for _, expected := range []string{"shared-data", "spire-agent-socket", "spiffe-helper-config", "svid-output", "envoy-config", AuthproxyRoutesConfigMapName, "authbridge-runtime-config"} {
 		if !names[expected] {
 			t.Errorf("missing volume %q", expected)
 		}
@@ -246,3 +246,77 @@ func TestOverrideEnvoyConfigMapInVolumes(t *testing.T) {
 		})
 	}
 }
+
+// TestOverrideRoutesConfigMapInVolumes verifies the per-agent routes override:
+// when AgentRuntime has spec.auth.outbound routes, the authproxy-routes volume
+// is redirected to authbridge-routes-<crName> without mutating the input.
+func TestOverrideRoutesConfigMapInVolumes(t *testing.T) {
+	tests := []struct {
+		name    string
+		volumes func() []corev1.Volume
+		newCM   string
+		found   bool
+	}{
+		{
+			name: "volume found, name swapped",
+			volumes: func() []corev1.Volume {
+				return BuildRequiredVolumes()
+			},
+			newCM: "authbridge-routes-my-agent",
+			found: true,
+		},
+		{
+			name: "no authproxy-routes volume, list unchanged",
+			volumes: func() []corev1.Volume {
+				return []corev1.Volume{{
+					Name:         "shared-data",
+					VolumeSource: corev1.VolumeSource{EmptyDir: &corev1.EmptyDirVolumeSource{}},
+				}}
+			},
+			newCM: "authbridge-routes-my-agent",
+			found: false,
+		},
+	}
+
+	for _, tt := range tests {
+		t.Run(tt.name, func(t *testing.T) {
+			original := tt.volumes()
+			overridden := overrideRoutesConfigMapInVolumes(original, tt.newCM)
+
+			// Original must not be mutated
+			for _, v := range original {
+				if v.Name == AuthproxyRoutesConfigMapName && v.ConfigMap != nil {
+					if v.ConfigMap.Name != AuthproxyRoutesConfigMapName {
+						t.Errorf("original was mutated: got %q", v.ConfigMap.Name)
+					}
+				}
+			}
+
+			// Output length matches input length
+			if len(overridden) != len(original) {
+				t.Fatalf("overridden length = %d, want %d", len(overridden), len(original))
+			}
+
+			// Find-and-swap behavior
+			swappedFound := false
+			for _, v := range overridden {
+				if v.Name == AuthproxyRoutesConfigMapName && v.ConfigMap != nil {
+					swappedFound = true
+					if v.ConfigMap.Name != tt.newCM {
+						t.Errorf("%s CM name = %q, want %q", AuthproxyRoutesConfigMapName, v.ConfigMap.Name, tt.newCM)
+					}
+					// Verify Optional is set to false for per-agent routes
+					if v.ConfigMap.Optional == nil || *v.ConfigMap.Optional != false {
+						t.Errorf("%s Optional should be false when overridden", AuthproxyRoutesConfigMapName)
+					}
+				}
+			}
+			if tt.found && !swappedFound {
+				t.Fatalf("expected %s volume in overridden but didn't find it", AuthproxyRoutesConfigMapName)
+			}
+			if !tt.found && swappedFound {
+				t.Fatalf("%s volume should not have been added", AuthproxyRoutesConfigMapName)
+			}
+		})
+	}
+}