diff --git a/src/System.Windows.Forms/System/Windows/Forms/Controls/ToolStrips/ToolStrip.cs b/src/System.Windows.Forms/System/Windows/Forms/Controls/ToolStrips/ToolStrip.cs
index 893d5ad4c31..f4f638093f6 100644
--- a/src/System.Windows.Forms/System/Windows/Forms/Controls/ToolStrips/ToolStrip.cs
+++ b/src/System.Windows.Forms/System/Windows/Forms/Controls/ToolStrips/ToolStrip.cs
@@ -3940,7 +3940,7 @@ internal override void ReleaseUiaProvider(HWND handle)
     /// <param name="items">contains ToolStrip or ToolStripDropDown items to disconnect</param>
     internal virtual void ReleaseToolStripItemsProviders(ToolStripItemCollection items)
     {
-        ToolStripItem[] itemsArray = [..items.Cast<ToolStripItem>()];
+        ToolStripItem[] itemsArray = [.. items.Cast<ToolStripItem>()];
         foreach (ToolStripItem toolStripItem in itemsArray)
         {
             if (toolStripItem is ToolStripDropDownItem dropDownItem && dropDownItem.DropDownItems.Count > 0)
@@ -4585,8 +4585,48 @@ protected override void WndProc(ref Message m)
         {
             SnapFocus((HWND)(nint)m.WParamInternal);
 
-            // For fix https://github.com/dotnet/winforms/issues/12916
-            ToolStripManager.ModalMenuFilter.SetActiveToolStrip(this);
+            if (IsDropDown)
+            {
+                // Designer SmartTag panels are hosted in ToolStripDropDown. Keep these
+                // participating in modal menu tracking regardless of previous focus.
+                ToolStripManager.ModalMenuFilter.SetActiveToolStrip(this);
+            }
+
+            // Only activate ModalMenuFilter when focus transfers
+            // between ToolStrips (to fix #12916).
+            // Do NOT activate on generic Tab focus (#14489).
+            else
+            {
+                HWND previousFocus = (HWND)(nint)m.WParamInternal;
+                Control? previousControl = FromChildHandle(previousFocus);
+                if (previousControl is ToolStrip || previousControl?.Parent is ToolStrip)
+                {
+                    ToolStripManager.ModalMenuFilter.SetActiveToolStrip(this);
+                }
+            }
+        }
+
+        if (m.MsgInternal == PInvokeCore.WM_KILLFOCUS)
+        {
+            // Clear modal menu tracking when focus leaves ToolStrip context so
+            // keyboard input is not incorrectly routed after tabbing away.
+            // Keep ToolStripDropDowns in menu tracking while they remain visible (for
+            // example, designer SmartTag panels that may temporarily transfer focus).
+            if (!IsDropDown)
+            {
+                HWND nextFocus = (HWND)(nint)m.WParamInternal;
+                Control? nextControl = FromChildHandle(nextFocus);
+                if (ToolStripManager.ModalMenuFilter.GetActiveToolStrip() == this
+                    && nextControl is not ToolStrip
+                    && nextControl?.Parent is not ToolStrip)
+                {
+                    ToolStripManager.ModalMenuFilter.RemoveActiveToolStrip(this);
+                    if (ToolStripManager.ModalMenuFilter.GetActiveToolStrip() is null)
+                    {
+                        ToolStripManager.ModalMenuFilter.ExitMenuMode();
+                    }
+                }
+            }
         }
 
         if (!AllowClickThrough && m.MsgInternal == PInvokeCore.WM_MOUSEACTIVATE)
diff --git a/src/test/integration/UIIntegrationTests/ToolStripTests.cs b/src/test/integration/UIIntegrationTests/ToolStripTests.cs
index 7a72344c41a..baacf2f4f7c 100644
--- a/src/test/integration/UIIntegrationTests/ToolStripTests.cs
+++ b/src/test/integration/UIIntegrationTests/ToolStripTests.cs
@@ -16,6 +16,66 @@ public ToolStripTests(ITestOutputHelper testOutputHelper)
         _sharedImageList.Images.Add("square", Image.FromFile("./Resources/image.png"));
     }
 
+    // Regression test for https://github.com/dotnet/winforms/issues/14489
+    [WinFormsFact]
+    public async Task ToolStrip_TabFromTreeView_ThenBack_ArrowKeysStillGoToTreeView()
+    {
+        await RunFormAsync(
+            () =>
+            {
+                Form form = new()
+                {
+                    TopMost = true
+                };
+
+                TreeView treeView = new()
+                {
+                    Dock = DockStyle.Fill,
+                    TabIndex = 0,
+                    HideSelection = false
+                };
+                treeView.Nodes.Add("Node 1");
+                treeView.Nodes.Add("Node 2");
+                treeView.SelectedNode = treeView.Nodes[0];
+
+                ToolStrip toolStrip = new()
+                {
+                    Dock = DockStyle.Top,
+                    TabStop = true,
+                    TabIndex = 1
+                };
+                toolStrip.Items.Add(new ToolStripButton("Button"));
+
+                form.Controls.Add(treeView);
+                form.Controls.Add(toolStrip);
+
+                return (form, (treeView, toolStrip));
+            },
+            async (form, controls) =>
+            {
+                var (treeView, toolStrip) = controls;
+
+                treeView.Focus();
+                await WaitForIdleAsync();
+                Assert.True(treeView.Focused);
+                Assert.Equal(treeView.Nodes[0], treeView.SelectedNode);
+
+                Assert.True(form.SelectNextControl(treeView, forward: true, tabStopOnly: true, nested: true, wrap: true));
+                await WaitForIdleAsync();
+                Assert.True(toolStrip.Focused);
+
+                Assert.True(form.SelectNextControl(toolStrip, forward: false, tabStopOnly: true, nested: true, wrap: true));
+                await WaitForIdleAsync();
+                Assert.True(treeView.Focused);
+
+                treeView.Focus();
+                await WaitForIdleAsync();
+                Assert.True(treeView.Focused);
+                Assert.Same(treeView, form.ActiveControl);
+                Assert.Equal(treeView.Nodes[0], treeView.SelectedNode);
+            });
+    }
+
     // Regression test for https://github.com/dotnet/winforms/issues/6881
     [WinFormsFact]
     public void ToolStrip_shared_imagelist_should_not_get_disposed_when_toolstrip_does()
diff --git a/src/test/unit/System.Windows.Forms/System/Windows/Forms/ToolStripTests.cs b/src/test/unit/System.Windows.Forms/System/Windows/Forms/ToolStripTests.cs
index 399936d9432..e9a0821250c 100644
--- a/src/test/unit/System.Windows.Forms/System/Windows/Forms/ToolStripTests.cs
+++ b/src/test/unit/System.Windows.Forms/System/Windows/Forms/ToolStripTests.cs
@@ -7226,6 +7226,38 @@ public void ToolStrip_WndProc_InvokeMouseHoverWithHandle_Success()
         Assert.Equal(0, createdCallCount);
     }
 
+    [WinFormsFact]
+    public void ToolStrip_WndProc_InvokeSetFocusFromToolStrip_ActivatesModalMenuFilter()
+    {
+        ToolStripManager.ModalMenuFilter.ExitMenuMode();
+
+        using Form form = new();
+        using SubToolStrip previousToolStrip = new() { TabStop = true };
+        using SubToolStrip currentToolStrip = new() { TabStop = true };
+
+        form.Controls.Add(previousToolStrip);
+        form.Controls.Add(currentToolStrip);
+
+        _ = form.Handle;
+        _ = previousToolStrip.Handle;
+        _ = currentToolStrip.Handle;
+
+        try
+        {
+            Message m = Message.Create(currentToolStrip.Handle, (int)PInvokeCore.WM_SETFOCUS, previousToolStrip.Handle, IntPtr.Zero);
+            currentToolStrip.WndProc(ref m);
+
+            Assert.Same(currentToolStrip, ToolStripManager.ModalMenuFilter.GetActiveToolStrip());
+            Assert.True(ToolStripManager.ModalMenuFilter.InMenuMode);
+        }
+        finally
+        {
+            ToolStripManager.ModalMenuFilter.RemoveActiveToolStrip(currentToolStrip);
+            ToolStripManager.ModalMenuFilter.RemoveActiveToolStrip(previousToolStrip);
+            ToolStripManager.ModalMenuFilter.ExitMenuMode();
+        }
+    }
+
     [WinFormsFact]
     public void ToolStrip_KeyboardAccelerators_ReturnsExpected()
     {