diff --git a/cli-plugins/socket/socket.go b/cli-plugins/socket/socket.go
index b9b297fa06db..9724c4e7f0e9 100644
--- a/cli-plugins/socket/socket.go
+++ b/cli-plugins/socket/socket.go
@@ -90,6 +90,16 @@ func (pl *PluginServer) Addr() net.Addr {
 	return pl.l.Addr()
 }
 
+// HasConnections reports whether any plugin has connected to the server.
+func (pl *PluginServer) HasConnections() bool {
+	if pl == nil {
+		return false
+	}
+	pl.mu.Lock()
+	defer pl.mu.Unlock()
+	return len(pl.conns) > 0
+}
+
 // Close ensures that the server is no longer accepting new connections and
 // closes all existing connections. Existing connections will receive [io.EOF].
 //
diff --git a/cmd/docker/docker.go b/cmd/docker/docker.go
index 0efcc70118fe..d6592ef2b555 100644
--- a/cmd/docker/docker.go
+++ b/cmd/docker/docker.go
@@ -368,10 +368,22 @@ func tryPluginRun(ctx context.Context, dockerCli command.Cli, cmd *cobra.Command
 		//
 		// Repeated invocations result in EINVAL or EBADF,
 		// but that is fine for our purposes.
+		hasSocketConnections := srv != nil && srv.HasConnections()
 		if srv != nil {
 			_ = srv.Close()
 		}
 
+		// Plugins using the CLI plugin socket are notified by closing the
+		// server connections above. Older plugins do not connect to the socket,
+		// so forward the user's termination signal directly to let them shut down
+		// gracefully instead of leaving them running in the background.
+		if !force && !hasSocketConnections {
+			var signalErr errCtxSignalTerminated
+			if errors.As(context.Cause(ctx), &signalErr) && signalErr.signal != os.Interrupt && plugincmd.Process != nil {
+				_ = plugincmd.Process.Signal(signalErr.signal)
+			}
+		}
+
 		// force the process to terminate if it hasn't already
 		if force {
 			// Close forceExitCh before Kill so the channel is guaranteed
@@ -387,11 +399,11 @@ func tryPluginRun(ctx context.Context, dockerCli command.Cli, cmd *cobra.Command
 		retries := 0
 		// catch the first signal through context cancellation
 		<-ctx.Done()
-		tryTerminatePlugin(false)
-
-		// register subsequent signals
+		// Register subsequent signals before attempting graceful termination, so
+		// quick repeated signals are still observed while cleanup is in progress.
 		signals := make(chan os.Signal, exitLimit)
 		signal.Notify(signals, platformsignals.TerminationSignals...)
+		tryTerminatePlugin(false)
 
 		force := false
 		for range signals {
diff --git a/e2e/cli-plugins/plugins/presocket/main.go b/e2e/cli-plugins/plugins/presocket/main.go
index d1a4b3501175..cd12d49d7918 100644
--- a/e2e/cli-plugins/plugins/presocket/main.go
+++ b/e2e/cli-plugins/plugins/presocket/main.go
@@ -55,6 +55,19 @@ func RootCmd(dockerCli command.Cli) *cobra.Command {
 		},
 	})
 
+	cmd.AddCommand(&cobra.Command{
+		Use:   "test-no-socket-exit-on-signal",
+		Short: "test command that exits when it receives a termination signal",
+		RunE: func(cmd *cobra.Command, args []string) error {
+			signalCh := make(chan os.Signal, 1)
+			signal.Notify(signalCh, syscall.SIGINT, syscall.SIGTERM)
+			sig := <-signalCh
+			_, _ = fmt.Fprintln(dockerCli.Out(), "received", sig)
+			os.Exit(2)
+			return nil
+		},
+	})
+
 	cmd.AddCommand(&cobra.Command{
 		Use:   "test-socket",
 		Short: "test command that runs until it receives a SIGINT",
diff --git a/e2e/cli-plugins/socket_test.go b/e2e/cli-plugins/socket_test.go
index 2bb93dd8f2a6..1a4e983144f7 100644
--- a/e2e/cli-plugins/socket_test.go
+++ b/e2e/cli-plugins/socket_test.go
@@ -179,6 +179,31 @@ func TestPluginSocketCommunication(t *testing.T) {
 	})
 
 	t.Run("detached", func(t *testing.T) {
+		t.Run("the plugin receives SIGTERM sent directly to the CLI", func(t *testing.T) {
+			cmd := run("presocket", "test-no-socket-exit-on-signal")
+			command := exec.Command(cmd.Command[0], cmd.Command[1:]...)
+			t.Log(strings.Join(command.Args, " "))
+			command.SysProcAttr = &syscall.SysProcAttr{
+				Setpgid: true,
+			}
+
+			go func() {
+				<-time.After(time.Second)
+				// Signal the CLI process directly, not the process group. When a
+				// plugin is detached and cannot be canceled over the plugin socket,
+				// the CLI should forward the termination signal to the plugin.
+				err := syscall.Kill(command.Process.Pid, syscall.SIGTERM)
+				assert.NilError(t, err, "failed to signal CLI process")
+			}()
+			out, err := command.CombinedOutput()
+
+			var exitError *exec.ExitError
+			assert.Assert(t, errors.As(err, &exitError))
+			assert.Check(t, exitError.Exited())
+			assert.Check(t, is.Equal(exitError.ExitCode(), 2))
+			assert.Equal(t, string(out), "received terminated\n")
+		})
+
 		t.Run("the plugin does not get signalled", func(t *testing.T) {
 			cmd := run("presocket", "test-socket")
 			command := exec.Command(cmd.Command[0], cmd.Command[1:]...)