diff --git a/cli/server.go b/cli/server.go
index be3a7fefd2..2880ea1088 100644
--- a/cli/server.go
+++ b/cli/server.go
@@ -653,6 +653,7 @@ func (r *RootCmd) Server(newAPI func(context.Context, *coderd.Options) (*coderd.
 			}
 
 			options := &coderd.Options{
+				ID:                          uuid.New(),
 				AccessURL:                   vals.AccessURL.Value(),
 				AppHostname:                 appHostname,
 				AppHostnameRegex:            appHostnameRegex,
diff --git a/enterprise/cli/server.go b/enterprise/cli/server.go
index 75db53bce2..9a2d930f7a 100644
--- a/enterprise/cli/server.go
+++ b/enterprise/cli/server.go
@@ -13,7 +13,6 @@ import (
 	"net/url"
 	"time"
 
-	"github.com/google/uuid"
 	"golang.org/x/xerrors"
 	"tailscale.com/derp"
 	"tailscale.com/types/key"
@@ -138,10 +137,8 @@ func (r *RootCmd) Server(_ func()) *serpent.Command {
 		if err != nil {
 			return nil, nil, xerrors.Errorf("create DERP mesh TLS config: %w", err)
 		}
-		replicaID := uuid.New()
-		options.ID = replicaID
 		replicaManager, err := replicasync.New(ctx, options.Logger, options.Database, options.Pubsub, &replicasync.Options{
-			ID:           replicaID,
+			ID:           options.ID,
 			RelayAddress: options.DeploymentValues.DERP.Server.RelayURL.String(),
 			// #nosec G115 - DERP region IDs are small and fit in int32
 			RegionID:       int32(options.DeploymentValues.DERP.Server.RegionID.Value()),
diff --git a/enterprise/coderd/coderd.go b/enterprise/coderd/coderd.go
index fc4484a23f..d71c8d27d5 100644
--- a/enterprise/coderd/coderd.go
+++ b/enterprise/coderd/coderd.go
@@ -226,11 +226,8 @@ func New(ctx context.Context, options *Options) (_ *API, err error) {
 
 	// The API replica ID must match the replica manager ID because other
 	// replicas use this ID to relay work back to the owning API instance.
-	if options.ReplicaManager == nil {
-		return nil, xerrors.New("replica manager is required")
-	}
-	if options.Options.ID == uuid.Nil {
-		options.Options.ID = options.ReplicaManager.ID()
+	if options.Options.ID != options.ReplicaManager.ID() {
+		return nil, xerrors.Errorf("replica manager ID %s does not match coderd ID %s", options.ReplicaManager.ID(), options.Options.ID)
 	}
 
 	api := &API{
diff --git a/enterprise/coderd/coderdenttest/coderdenttest.go b/enterprise/coderd/coderdenttest/coderdenttest.go
index a5d3aac942..b9ba156394 100644
--- a/enterprise/coderd/coderdenttest/coderdenttest.go
+++ b/enterprise/coderd/coderdenttest/coderdenttest.go
@@ -105,10 +105,17 @@ func NewWithAPI(t *testing.T, options *Options) (
 	}
 	require.False(t, options.DontAddFirstUser && !options.DontAddLicense, "DontAddFirstUser requires DontAddLicense")
 	setHandler, cancelFunc, serverURL, oop := coderdtest.NewOptions(t, options.Options)
+	if oop.ID == uuid.Nil {
+		oop.ID = uuid.New()
+	}
 	replicaManager := options.ReplicaManager
+	if replicaManager != nil {
+		oop.ID = replicaManager.ID()
+	}
 	if replicaManager == nil {
 		var err error
 		replicaManager, err = replicasync.New(context.Background(), oop.Logger, oop.Database, oop.Pubsub, &replicasync.Options{
+			ID:           oop.ID,
 			RelayAddress: serverURL.String(),
 			// #nosec G115 - DERP region IDs are small and fit in int32.
 			RegionID:       int32(oop.DeploymentValues.DERP.Server.RegionID.Value()),