diff --git a/src/System.Windows.Forms/System/Windows/Forms/Controls/ComboBox/ComboBox.ComboBoxChildNativeWindow.cs b/src/System.Windows.Forms/System/Windows/Forms/Controls/ComboBox/ComboBox.ComboBoxChildNativeWindow.cs
index 60b17e60db7..0ff802ec8e9 100644
--- a/src/System.Windows.Forms/System/Windows/Forms/Controls/ComboBox/ComboBox.ComboBoxChildNativeWindow.cs
+++ b/src/System.Windows.Forms/System/Windows/Forms/Controls/ComboBox/ComboBox.ComboBoxChildNativeWindow.cs
@@ -25,6 +25,18 @@ protected override unsafe void WndProc(ref Message m)
                 case PInvokeCore.WM_GETOBJECT:
                     WmGetObject(ref m);
                     return;
+                case PInvokeCore.WM_WINDOWPOSCHANGING:
+                    if (_childWindowType == ChildWindowType.DropDownList)
+                    {
+                        WmWindowPosChanging(ref m);
+                        DefWndProc(ref m);
+                    }
+                    else
+                    {
+                        _owner.ChildWndProc(ref m);
+                    }
+
+                    break;
                 case PInvokeCore.WM_MOUSEMOVE:
                     if (_childWindowType == ChildWindowType.DropDownList)
                     {
@@ -153,5 +165,23 @@ private unsafe void WmGetObject(ref Message m)
                 throw new InvalidOperationException(SR.RichControlLresult, e);
             }
         }
+
+        private unsafe void WmWindowPosChanging(ref Message m)
+        {
+            // The native ComboBox sizes the dropdown list during its own layout
+            // pass (after CBN_DROPDOWN fires). Intercept here to enforce the
+            // managed computed height before the OS commits the final size.
+            // This ensures the UI reflects Items.Count (or explicit DropDownHeight)
+            // even when the list is empty or items are cleared at runtime.
+            WINDOWPOS* pos = (WINDOWPOS*)(nint)m.LParamInternal;
+            if (pos is not null && (pos->flags & SET_WINDOW_POS_FLAGS.SWP_NOSIZE) == 0)
+            {
+                int height = _owner.GetCalculatedDropDownHeight();
+                if (pos->cy != height)
+                {
+                    pos->cy = height;
+                }
+            }
+        }
     }
 }
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 5e4422eaf9c..86e36af873c 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
@@ -3327,14 +3327,8 @@ public override string ToString()
         return $"{s}, Items.Count: {_itemsCollection?.Count ?? 0}";
     }
 
-    private void UpdateDropDownHeight()
+    private int GetCalculatedDropDownHeight()
     {
-        if (_dropDownHandle.IsNull)
-        {
-            return;
-        }
-
-        // Now use the DropDownHeight property instead of calculating the Height...
         int height = DropDownHeight;
         if (height == DefaultDropDownHeight)
         {
@@ -3343,6 +3337,19 @@ private void UpdateDropDownHeight()
             height = ItemHeight * count + 2;
         }
 
+        return height;
+    }
+
+    private void UpdateDropDownHeight()
+    {
+        if (_dropDownHandle.IsNull)
+        {
+            return;
+        }
+
+        // Now use the DropDownHeight property instead of calculating the Height...
+        int height = GetCalculatedDropDownHeight();
+
         PInvoke.SetWindowPos(
             _dropDownHandle,
             HWND.HWND_TOP,