diff --git a/internal/provider/kubernetes/controller_offline.go b/internal/provider/kubernetes/controller_offline.go
index f3bcdf15aa..bd13320c93 100644
--- a/internal/provider/kubernetes/controller_offline.go
+++ b/internal/provider/kubernetes/controller_offline.go
@@ -159,17 +159,23 @@ func newOfflineGatewayAPIClient(extensionPolicies []schema.GroupVersionKind) cli
 		WithScheme(scheme).
 		WithIndex(&gwapiv1.Gateway{}, classGatewayIndex, gatewayIndexFunc).
 		WithIndex(&gwapiv1.Gateway{}, secretGatewayIndex, secretGatewayIndexFunc).
+		WithIndex(&gwapiv1.ListenerSet{}, gatewayListenerSetIndex, gatewayListenerSetIndexFunc).
 		WithIndex(&gwapiv1.HTTPRoute{}, gatewayHTTPRouteIndex, gatewayHTTPRouteIndexFunc).
 		WithIndex(&gwapiv1.HTTPRoute{}, backendHTTPRouteIndex, backendHTTPRouteIndexFunc).
+		WithIndex(&gwapiv1.HTTPRoute{}, listenerSetHTTPRouteIndex, listenerSetHTTPRouteIndexFunc).
 		WithIndex(&gwapiv1.HTTPRoute{}, httpRouteFilterHTTPRouteIndex, httpRouteFilterHTTPRouteIndexFunc).
 		WithIndex(&gwapiv1.GRPCRoute{}, gatewayGRPCRouteIndex, gatewayGRPCRouteIndexFunc).
 		WithIndex(&gwapiv1.GRPCRoute{}, backendGRPCRouteIndex, backendGRPCRouteIndexFunc).
+		WithIndex(&gwapiv1.GRPCRoute{}, listenerSetGRPCRouteIndex, listenerSetGRPCRouteIndexFunc).
 		WithIndex(&gwapiv1a2.TCPRoute{}, gatewayTCPRouteIndex, gatewayTCPRouteIndexFunc).
 		WithIndex(&gwapiv1a2.TCPRoute{}, backendTCPRouteIndex, backendTCPRouteIndexFunc).
+		WithIndex(&gwapiv1a2.TCPRoute{}, listenerSetTCPRouteIndex, listenerSetTCPRouteIndexFunc).
 		WithIndex(&gwapiv1a2.UDPRoute{}, gatewayUDPRouteIndex, gatewayUDPRouteIndexFunc).
 		WithIndex(&gwapiv1a2.UDPRoute{}, backendUDPRouteIndex, backendUDPRouteIndexFunc).
+		WithIndex(&gwapiv1a2.UDPRoute{}, listenerSetUDPRouteIndex, listenerSetUDPRouteIndexFunc).
 		WithIndex(&gwapiv1.TLSRoute{}, gatewayTLSRouteIndex, gatewayTLSRouteIndexFunc).
 		WithIndex(&gwapiv1.TLSRoute{}, backendTLSRouteIndex, backendTLSRouteIndexFunc).
+		WithIndex(&gwapiv1.TLSRoute{}, listenerSetTLSRouteIndex, listenerSetTLSRouteIndexFunc).
 		WithIndex(&egv1a1.EnvoyProxy{}, backendEnvoyProxyTelemetryIndex, backendEnvoyProxyTelemetryIndexFunc).
 		WithIndex(&egv1a1.EnvoyProxy{}, secretEnvoyProxyIndex, secretEnvoyProxyIndexFunc).
 		WithIndex(&egv1a1.BackendTrafficPolicy{}, configMapBtpIndex, configMapBtpIndexFunc).
@@ -182,6 +188,7 @@ func newOfflineGatewayAPIClient(extensionPolicies []schema.GroupVersionKind) cli
 		WithIndex(&egv1a1.EnvoyExtensionPolicy{}, backendEnvoyExtensionPolicyIndex, backendEnvoyExtensionPolicyIndexFunc).
 		WithIndex(&egv1a1.EnvoyExtensionPolicy{}, secretEnvoyExtensionPolicyIndex, secretEnvoyExtensionPolicyIndexFunc).
 		WithIndex(&egv1a1.EnvoyExtensionPolicy{}, configMapEepIndex, configMapEepIndexFunc).
+		WithIndex(&egv1a1.EnvoyExtensionPolicy{}, clusterTrustBundleEepIndex, clusterTrustBundleEepIndexFunc).
 		WithIndex(&gwapiv1.BackendTLSPolicy{}, configMapBtlsIndex, configMapBtlsIndexFunc).
 		WithIndex(&gwapiv1.BackendTLSPolicy{}, secretBtlsIndex, secretBtlsIndexFunc).
 		WithIndex(&gwapiv1.BackendTLSPolicy{}, clusterTrustBundleBtlsIndex, clusterTrustBundleBtlsIndexFunc).
diff --git a/internal/provider/kubernetes/controller_offline_test.go b/internal/provider/kubernetes/controller_offline_test.go
index f64a29ce39..8f6198890a 100644
--- a/internal/provider/kubernetes/controller_offline_test.go
+++ b/internal/provider/kubernetes/controller_offline_test.go
@@ -141,11 +141,18 @@ func TestNewOfflineGatewayAPIControllerIndexRegistration(t *testing.T) {
 		require.NoError(t, err)
 	})
 
+	t.Run("ListenerSet index", func(t *testing.T) {
+		err := cli.List(context.Background(), &gwapiv1.ListenerSetList{}, client.MatchingFields{gatewayListenerSetIndex: "any"})
+		require.NoError(t, err)
+	})
+
 	t.Run("HTTPRoute indices", func(t *testing.T) {
 		err := cli.List(context.Background(), &gwapiv1.HTTPRouteList{}, client.MatchingFields{gatewayHTTPRouteIndex: "any"})
 		require.NoError(t, err)
 		err = cli.List(context.Background(), &gwapiv1.HTTPRouteList{}, client.MatchingFields{backendHTTPRouteIndex: "any"})
 		require.NoError(t, err)
+		err = cli.List(context.Background(), &gwapiv1.HTTPRouteList{}, client.MatchingFields{listenerSetHTTPRouteIndex: "any"})
+		require.NoError(t, err)
 		err = cli.List(context.Background(), &gwapiv1.HTTPRouteList{}, client.MatchingFields{httpRouteFilterHTTPRouteIndex: "any"})
 		require.NoError(t, err)
 	})
@@ -155,6 +162,8 @@ func TestNewOfflineGatewayAPIControllerIndexRegistration(t *testing.T) {
 		require.NoError(t, err)
 		err = cli.List(context.Background(), &gwapiv1.GRPCRouteList{}, client.MatchingFields{backendGRPCRouteIndex: "any"})
 		require.NoError(t, err)
+		err = cli.List(context.Background(), &gwapiv1.GRPCRouteList{}, client.MatchingFields{listenerSetGRPCRouteIndex: "any"})
+		require.NoError(t, err)
 	})
 
 	t.Run("TCPRoute indices", func(t *testing.T) {
@@ -162,6 +171,8 @@ func TestNewOfflineGatewayAPIControllerIndexRegistration(t *testing.T) {
 		require.NoError(t, err)
 		err = cli.List(context.Background(), &gwapiv1a2.TCPRouteList{}, client.MatchingFields{backendTCPRouteIndex: "any"})
 		require.NoError(t, err)
+		err = cli.List(context.Background(), &gwapiv1a2.TCPRouteList{}, client.MatchingFields{listenerSetTCPRouteIndex: "any"})
+		require.NoError(t, err)
 	})
 
 	t.Run("UDPRoute indices", func(t *testing.T) {
@@ -169,6 +180,8 @@ func TestNewOfflineGatewayAPIControllerIndexRegistration(t *testing.T) {
 		require.NoError(t, err)
 		err = cli.List(context.Background(), &gwapiv1a2.UDPRouteList{}, client.MatchingFields{backendUDPRouteIndex: "any"})
 		require.NoError(t, err)
+		err = cli.List(context.Background(), &gwapiv1a2.UDPRouteList{}, client.MatchingFields{listenerSetUDPRouteIndex: "any"})
+		require.NoError(t, err)
 	})
 
 	t.Run("TLSRoute indices", func(t *testing.T) {
@@ -176,6 +189,8 @@ func TestNewOfflineGatewayAPIControllerIndexRegistration(t *testing.T) {
 		require.NoError(t, err)
 		err = cli.List(context.Background(), &gwapiv1.TLSRouteList{}, client.MatchingFields{backendTLSRouteIndex: "any"})
 		require.NoError(t, err)
+		err = cli.List(context.Background(), &gwapiv1.TLSRouteList{}, client.MatchingFields{listenerSetTLSRouteIndex: "any"})
+		require.NoError(t, err)
 	})
 
 	t.Run("EnvoyProxy indices", func(t *testing.T) {
@@ -215,6 +230,8 @@ func TestNewOfflineGatewayAPIControllerIndexRegistration(t *testing.T) {
 		require.NoError(t, err)
 		err = cli.List(context.Background(), &egv1a1.EnvoyExtensionPolicyList{}, client.MatchingFields{configMapEepIndex: "any"})
 		require.NoError(t, err)
+		err = cli.List(context.Background(), &egv1a1.EnvoyExtensionPolicyList{}, client.MatchingFields{clusterTrustBundleEepIndex: "any"})
+		require.NoError(t, err)
 	})
 
 	t.Run("BackendTLSPolicy indices", func(t *testing.T) {
diff --git a/release-notes/current/bug_fixes/9320-offline-controller-listenerset-indexes.md b/release-notes/current/bug_fixes/9320-offline-controller-listenerset-indexes.md
new file mode 100644
index 0000000000..da8d964506
--- /dev/null
+++ b/release-notes/current/bug_fixes/9320-offline-controller-listenerset-indexes.md
@@ -0,0 +1 @@
+Fixed the standalone offline controller used by the File provider to register the missing ListenerSet, ListenerSet-owned route, and ClusterTrustBundle EnvoyExtensionPolicy indexes so reconciliation no longer fails with unregistered index errors.