diff --git a/internal/devserver/server.go b/internal/devserver/server.go
index 52756e0ae..d55824c54 100644
--- a/internal/devserver/server.go
+++ b/internal/devserver/server.go
@@ -47,13 +47,13 @@ import (
 	"go.temporal.io/server/common/metrics"
 	sqliteplugin "go.temporal.io/server/common/persistence/sql/sqlplugin/sqlite"
 	"go.temporal.io/server/common/primitives"
-	"go.temporal.io/server/components/callbacks"
 	"go.temporal.io/server/components/nexusoperations"
 	"go.temporal.io/server/schema/sqlite"
 	sqliteschema "go.temporal.io/server/schema/sqlite"
 	"go.temporal.io/server/temporal"
 	"google.golang.org/grpc"
 	"gopkg.in/yaml.v3"
+	"go.temporal.io/server/components/callbacks"
 )
 
 const (
@@ -241,19 +241,10 @@ func (s *StartOptions) buildServerOptions() ([]temporal.ServerOption, *slog.Leve
 	dynConf[dynamicconfig.HistoryCacheHostLevelMaxSize.Key()] = 8096
 	// Up default visibility RPS
 	dynConf[dynamicconfig.FrontendMaxNamespaceVisibilityRPSPerInstance.Key()] = 100
-	// NOTE that the URL scheme is fixed to HTTP since the dev server doesn't support TLS at the time of writing.
-	dynConf[nexusoperations.CallbackURLTemplate.Key()] = fmt.Sprintf(
-		"http://%s:%d/namespaces/{{.NamespaceName}}/nexus/callback", MaybeEscapeIPv6(s.FrontendIP), s.FrontendHTTPPort)
-	dynConf[callbacks.AllowedAddresses.Key()] = []struct {
-		Pattern       string
-		AllowInsecure bool
-	}{
-		{
-			Pattern:       fmt.Sprintf("%s:%d", MaybeEscapeIPv6(s.FrontendIP), s.FrontendHTTPPort),
-			AllowInsecure: true,
-		},
-	}
+	// Enable the system callback URL for worker targets.
+	dynConf[nexusoperations.UseSystemCallbackURL.Key()] = true
 
+	dynConf[callbacks.AllowedAddresses.Key()] = true
 	// Dynamic config if set
 	for k, v := range s.DynamicConfigValues {
 		dynConf[dynamicconfig.MakeKey(k)] = v
diff --git a/internal/temporalcli/commands.workflow_view_test.go b/internal/temporalcli/commands.workflow_view_test.go
index 980d4b632..5abb30068 100644
--- a/internal/temporalcli/commands.workflow_view_test.go
+++ b/internal/temporalcli/commands.workflow_view_test.go
@@ -757,7 +757,7 @@ func (s *SharedServerSuite) TestWorkflow_Describe_NexusOperationAndCallback() {
 	out = res.Stdout.String()
 	s.ContainsOnSameLine(out, "WorkflowId", handlerWorkflowID)
 	s.Contains(out, "Callbacks: 1")
-	s.ContainsOnSameLine(out, "URL", "http://"+s.DevServer.Options.FrontendIP)
+	s.ContainsOnSameLine(out, "URL", "temporal://system")
 	s.ContainsOnSameLine(out, "Trigger", "WorkflowClosed")
 	s.ContainsOnSameLine(out, "State", "Succeeded")
 
@@ -777,11 +777,11 @@ func (s *SharedServerSuite) TestWorkflow_Describe_NexusOperationAndCallback() {
 func (s *SharedServerSuite) TestWorkflow_Describe_NexusOperationBlocked() {
 	endpointName := validEndpointName(s.T())
 
-	// Call an unreachable operation from this workflow.
+	// Call an operation that has no handler registered.
 	callerWorkflow := func(ctx workflow.Context) error {
 		client := workflow.NewNexusClient(endpointName, "test-service")
 		fut := client.ExecuteOperation(ctx, "test-op", nil, workflow.NexusOperationOptions{})
-		// Destination is unreachable, the future will never complete.
+		// No handler is registered, the operation will fail and trigger the circuit breaker.
 		return fut.GetNexusOperationExecution().Get(ctx, nil)
 	}
 
@@ -790,16 +790,19 @@ func (s *SharedServerSuite) TestWorkflow_Describe_NexusOperationBlocked() {
 	})
 	defer w.Stop()
 
-	// Create an endpoint for this test.
+	// Create an endpoint for this test pointing to a worker target.
+	// The worker has no handler for "test-service"/"test-op", so requests will fail
+	// and eventually trigger the circuit breaker.
 	_, err := s.Client.OperatorService().CreateNexusEndpoint(
 		s.Context,
 		&operatorservice.CreateNexusEndpointRequest{
 			Spec: &nexuspb.EndpointSpec{
 				Name: endpointName,
 				Target: &nexuspb.EndpointTarget{
-					Variant: &nexuspb.EndpointTarget_External_{
-						External: &nexuspb.EndpointTarget_External{
-							Url: "http://localhost:12345", // unreachable destination
+					Variant: &nexuspb.EndpointTarget_Worker_{
+						Worker: &nexuspb.EndpointTarget_Worker{
+							Namespace: s.Namespace(),
+							TaskQueue: w.Options.TaskQueue,
 						},
 					},
 				},
@@ -808,7 +811,6 @@ func (s *SharedServerSuite) TestWorkflow_Describe_NexusOperationBlocked() {
 	)
 	s.NoError(err)
 
-	// Start the workflow and wait until the operation is started.
 	run, err := s.Client.ExecuteWorkflow(
 		s.Context,
 		client.StartWorkflowOptions{TaskQueue: w.Options.TaskQueue},
@@ -847,7 +849,6 @@ func (s *SharedServerSuite) TestWorkflow_Describe_NexusOperationBlocked() {
 	s.ContainsOnSameLine(out, "Operation", "test-op")
 	s.ContainsOnSameLine(out, "BlockedReason", "The circuit breaker is open.")
 
-	// Operations - JSON
 	res = s.Execute(
 		"workflow", "describe",
 		"--address", s.Address(),