diff --git a/src/System.Windows.Forms/System/Windows/Forms/Controls/ComboBox/ComboBox.Modern.cs b/src/System.Windows.Forms/System/Windows/Forms/Controls/ComboBox/ComboBox.Modern.cs
index 90eeab9368b..766c40d952d 100644
--- a/src/System.Windows.Forms/System/Windows/Forms/Controls/ComboBox/ComboBox.Modern.cs
+++ b/src/System.Windows.Forms/System/Windows/Forms/Controls/ComboBox/ComboBox.Modern.cs
@@ -654,12 +654,23 @@ protected override void OnVisualStylesModeChanged(EventArgs e)
         ResetComboAdapter();
         ResetHeightCache();
 
+        bool recreateSystemHandle = FlatStyle == FlatStyle.System
+            && IsHandleCreated;
+
         // Crossing the modern/classic boundary is reported as VisualStylesModeChangeImpact.Recreate
         // (see GetVisualStylesModeChangeImpact), so the base recreates the handle here. That is the
         // only clean way to unwind the modern native-window state (the WM_NCCALCSIZE client
         // expansion and the per-handle modern baseline); a fresh classic handle then behaves exactly
         // as before, and a fresh modern handle captures a clean baseline.
+        // FlatStyle.System stays native, but an existing native handle still needs a rebuild when
+        // visual-style mode changes to avoid stale geometry in designer/runtime transitions.
         base.OnVisualStylesModeChanged(e);
+
+        if (recreateSystemHandle && IsHandleCreated)
+        {
+            RecreateHandle();
+        }
+
         ApplyModernComboLayout();
         RefreshModernDropDownCornerPreference();
     }
diff --git a/src/System.Windows.Forms/System/Windows/Forms/Controls/ComboBox/ComboBox.cs b/src/System.Windows.Forms/System/Windows/Forms/Controls/ComboBox/ComboBox.cs
index 3fe91f3fd09..fca5b5c33ef 100644
--- a/src/System.Windows.Forms/System/Windows/Forms/Controls/ComboBox/ComboBox.cs
+++ b/src/System.Windows.Forms/System/Windows/Forms/Controls/ComboBox/ComboBox.cs
@@ -530,15 +530,25 @@ public partial FlatStyle FlatStyle
                 return;
             }
 
-            bool usedModernMetrics = UsesModernComboAdapter;
+            bool previousUsesModernMetrics = UsesModernComboAdapter;
             _flatStyle = value;
             ResetComboAdapter();
 
-            if (usedModernMetrics != UsesModernComboAdapter)
+            bool currentUsesModernMetrics = UsesModernComboAdapter;
+
+            if (previousUsesModernMetrics != currentUsesModernMetrics)
             {
                 ResetHeightCache();
                 CommonProperties.xClearPreferredSizeCache(this);
-                ApplyModernComboLayout();
+
+                if (IsHandleCreated)
+                {
+                    RecreateHandle();
+                }
+                else
+                {
+                    ApplyModernComboLayout();
+                }
 
                 LayoutTransaction.DoLayout(
                     this,
@@ -553,8 +563,11 @@ public partial FlatStyle FlatStyle
                         PropertyNames.FlatStyle);
                 }
             }
+            else
+            {
+                ApplyModernComboLayout();
+            }
 
-            ApplyModernComboLayout();
             RefreshModernDropDownCornerPreference();
             Invalidate();
         }
diff --git a/src/test/unit/System.Windows.Forms/System/Windows/Forms/ComboBoxTests.cs b/src/test/unit/System.Windows.Forms/System/Windows/Forms/ComboBoxTests.cs
index 2af7ac2f04d..a9477200bc6 100644
--- a/src/test/unit/System.Windows.Forms/System/Windows/Forms/ComboBoxTests.cs
+++ b/src/test/unit/System.Windows.Forms/System/Windows/Forms/ComboBoxTests.cs
@@ -287,6 +287,64 @@ public void ComboBox_ModernVisualStyles_SystemModeChangeDoesNotRequestLayout()
         Assert.False(control.IsHandleCreated);
     }
 
+    [WinFormsFact]
+    public void ComboBox_ModernVisualStyles_FlatStyleTransitionToSystem_RecreatesHandle()
+    {
+        using SystemVisualSettingsTestScope settingsScope = new(
+            clientAreaAnimationEnabled: false,
+            highContrastEnabled: false);
+        using Panel parent = new();
+        using VisualStylesComboBox control = new()
+        {
+            FlatStyle = FlatStyle.Standard,
+            VisualStylesMode = VisualStylesMode.Net11
+        };
+        parent.Controls.Add(control);
+        parent.CreateControl();
+        control.CreateControl();
+
+        int handleCreatedCallCount = 0;
+        int handleDestroyedCallCount = 0;
+        control.HandleCreated += (sender, e) => handleCreatedCallCount++;
+        control.HandleDestroyed += (sender, e) => handleDestroyedCallCount++;
+
+        control.FlatStyle = FlatStyle.System;
+
+        Assert.True(control.IsHandleCreated);
+        Assert.Equal(1, handleDestroyedCallCount);
+        Assert.Equal(1, handleCreatedCallCount);
+        Assert.IsType<FlatComboAdapter>(control.CreateAdapter());
+    }
+
+    [WinFormsFact]
+    public void ComboBox_ModernVisualStyles_SystemModeBoundaryChangeWithHandle_RecreatesHandle()
+    {
+        using SystemVisualSettingsTestScope settingsScope = new(
+            clientAreaAnimationEnabled: false,
+            highContrastEnabled: false);
+        using Panel parent = new();
+        using VisualStylesComboBox control = new()
+        {
+            FlatStyle = FlatStyle.System,
+            VisualStylesMode = VisualStylesMode.Classic
+        };
+        parent.Controls.Add(control);
+        parent.CreateControl();
+        control.CreateControl();
+
+        int handleCreatedCallCount = 0;
+        int handleDestroyedCallCount = 0;
+        control.HandleCreated += (sender, e) => handleCreatedCallCount++;
+        control.HandleDestroyed += (sender, e) => handleDestroyedCallCount++;
+
+        control.VisualStylesMode = VisualStylesMode.Net11;
+
+        Assert.True(control.IsHandleCreated);
+        Assert.Equal(1, handleDestroyedCallCount);
+        Assert.Equal(1, handleCreatedCallCount);
+        Assert.IsType<FlatComboAdapter>(control.CreateAdapter());
+    }
+
     [WinFormsFact]
     public void ComboBox_ModernVisualStyles_ModeChangeRemeasuresAutoSizeRow()
     {