diff --git a/cli/ssh.go b/cli/ssh.go
index 990b972309..21437ee6ae 100644
--- a/cli/ssh.go
+++ b/cli/ssh.go
@@ -876,6 +876,7 @@ type closerStack struct {
 	closed  bool
 	logger  slog.Logger
 	err     error
+	wg      sync.WaitGroup
 }
 
 func newCloserStack(ctx context.Context, logger slog.Logger) *closerStack {
@@ -893,10 +894,13 @@ func (c *closerStack) close(err error) {
 	c.Lock()
 	if c.closed {
 		c.Unlock()
+		c.wg.Wait()
 		return
 	}
 	c.closed = true
 	c.err = err
+	c.wg.Add(1)
+	defer c.wg.Done()
 	c.Unlock()
 
 	for i := len(c.closers) - 1; i >= 0; i-- {
diff --git a/cli/ssh_internal_test.go b/cli/ssh_internal_test.go
index 0630deb36d..b612dd5ef9 100644
--- a/cli/ssh_internal_test.go
+++ b/cli/ssh_internal_test.go
@@ -4,6 +4,7 @@ import (
 	"context"
 	"net/url"
 	"testing"
+	"time"
 
 	"github.com/stretchr/testify/assert"
 	"github.com/stretchr/testify/require"
@@ -127,6 +128,43 @@ func TestCloserStack_PushAfterClose(t *testing.T) {
 	require.Equal(t, []*fakeCloser{fc1, fc0}, *closes, "should close fc1")
 }
 
+func TestCloserStack_CloseAfterContext(t *testing.T) {
+	t.Parallel()
+	testCtx := testutil.Context(t, testutil.WaitShort)
+	ctx, cancel := context.WithCancel(testCtx)
+	defer cancel()
+	logger := slogtest.Make(t, &slogtest.Options{IgnoreErrors: true}).Leveled(slog.LevelDebug)
+	uut := newCloserStack(ctx, logger)
+	ac := &asyncCloser{
+		t:        t,
+		ctx:      testCtx,
+		complete: make(chan struct{}),
+		started:  make(chan struct{}),
+	}
+	err := uut.push("async", ac)
+	require.NoError(t, err)
+	cancel()
+	testutil.RequireRecvCtx(testCtx, t, ac.started)
+
+	closed := make(chan struct{})
+	go func() {
+		defer close(closed)
+		uut.close(nil)
+	}()
+
+	// since the asyncCloser is still waiting, we shouldn't complete uut.close()
+	select {
+	case <-time.After(testutil.IntervalFast):
+		// OK!
+	case <-closed:
+		t.Fatal("closed before stack was finished")
+	}
+
+	// complete the asyncCloser
+	close(ac.complete)
+	testutil.RequireRecvCtx(testCtx, t, closed)
+}
+
 type fakeCloser struct {
 	closes *[]*fakeCloser
 	err    error
@@ -136,3 +174,21 @@ func (c *fakeCloser) Close() error {
 	*c.closes = append(*c.closes, c)
 	return c.err
 }
+
+type asyncCloser struct {
+	t        *testing.T
+	ctx      context.Context
+	started  chan struct{}
+	complete chan struct{}
+}
+
+func (c *asyncCloser) Close() error {
+	close(c.started)
+	select {
+	case <-c.ctx.Done():
+		c.t.Error("timed out")
+		return c.ctx.Err()
+	case <-c.complete:
+		return nil
+	}
+}