diff --git a/go/cmd/vtctldclient/command/root.go b/go/cmd/vtctldclient/command/root.go
index 8a03eadc764..742944315f1 100644
--- a/go/cmd/vtctldclient/command/root.go
+++ b/go/cmd/vtctldclient/command/root.go
@@ -23,6 +23,7 @@ import (
 	"io"
 	"strconv"
 	"strings"
+	"sync"
 	"time"
 
 	"github.com/spf13/cobra"
@@ -70,6 +71,11 @@ var (
 	// Register functions to be called when the command completes.
 	onTerm = []func(){}
 
+	// Register our nil tmclient grpc handler only one time.
+	// This is primarily for tests where we execute the root
+	// command multiple times.
+	once = sync.Once{}
+
 	server        string
 	actionTimeout time.Duration
 	compactOutput bool
@@ -194,9 +200,12 @@ func getClientForCommand(cmd *cobra.Command) (vtctldclient.VtctldClient, error)
 		onTerm = append(onTerm, ts.Close)
 
 		// Use internal vtcltd server implementation.
-		// Register a nil grpc handler -- we will not use tmclient at all.
-		tmclient.RegisterTabletManagerClientFactory("grpc", func() tmclient.TabletManagerClient {
-			return nil
+		// Register a nil grpc handler -- we will not use tmclient at all but
+		// a factory still needs to be registered.
+		once.Do(func() {
+			tmclient.RegisterTabletManagerClientFactory("grpc", func() tmclient.TabletManagerClient {
+				return nil
+			})
 		})
 		vtctld := grpcvtctldserver.NewVtctldServer(ts)
 		localvtctldclient.SetServer(vtctld)
diff --git a/go/cmd/vtctldclient/command/root_test.go b/go/cmd/vtctldclient/command/root_test.go
index 155fac78705..5efe844e1a1 100644
--- a/go/cmd/vtctldclient/command/root_test.go
+++ b/go/cmd/vtctldclient/command/root_test.go
@@ -17,13 +17,19 @@ limitations under the License.
 package command_test
 
 import (
+	"context"
+	"fmt"
 	"os"
+	"strings"
 	"testing"
+	"time"
 
 	"github.com/stretchr/testify/assert"
 	"github.com/stretchr/testify/require"
 
 	"vitess.io/vitess/go/cmd/vtctldclient/command"
+	"vitess.io/vitess/go/vt/topo"
+	"vitess.io/vitess/go/vt/topo/memorytopo"
 	"vitess.io/vitess/go/vt/vtctl/localvtctldclient"
 
 	vtctlservicepb "vitess.io/vitess/go/vt/proto/vtctlservice"
@@ -52,3 +58,64 @@ func TestRoot(t *testing.T) {
 		assert.Contains(t, err.Error(), "unknown command")
 	})
 }
+
+// TestRootWithInternalVtctld tests that the internal VtctldServer
+// implementation -- used with --server=internal -- works for
+// commands as expected.
+func TestRootWithInternalVtctld(t *testing.T) {
+	ctx, cancel := context.WithTimeout(context.Background(), 30*time.Second)
+	defer cancel()
+	cell := "zone1"
+	ts, factory := memorytopo.NewServerAndFactory(ctx, cell)
+	topo.RegisterFactory("test", factory)
+	command.VtctldClientProtocol = "local"
+	baseArgs := []string{"vtctldclient", "--server", "internal", "--topo-implementation", "test"}
+
+	args := append([]string{}, os.Args...)
+	protocol := command.VtctldClientProtocol
+	t.Cleanup(func() {
+		ts.Close()
+		os.Args = append([]string{}, args...)
+		command.VtctldClientProtocol = protocol
+	})
+
+	testCases := []struct {
+		command   string
+		args      []string
+		expectErr string
+	}{
+		{
+			command:   "AddCellInfo",
+			args:      []string{"--root", fmt.Sprintf("/vitess/%s", cell), "--server-address", "", cell},
+			expectErr: "node already exists", // Cell already exists
+		},
+		{
+			command: "GetTablets",
+		},
+		{
+			command:   "NoCommandDrJones",
+			expectErr: "unknown command", // Invalid command
+		},
+	}
+
+	for _, tc := range testCases {
+		t.Run(tc.command, func(t *testing.T) {
+			defer func() {
+				// Reset the OS args.
+				os.Args = append([]string{}, args...)
+			}()
+
+			os.Args = append(baseArgs, tc.command)
+			os.Args = append(os.Args, tc.args...)
+
+			err := command.Root.Execute()
+			if tc.expectErr != "" {
+				if !strings.Contains(err.Error(), tc.expectErr) {
+					t.Errorf(fmt.Sprintf("%s error = %v, expectErr = %v", tc.command, err, tc.expectErr))
+				}
+			} else {
+				require.NoError(t, err, "unexpected error: %v", err)
+			}
+		})
+	}
+}