diff --git a/src/System.Windows.Forms/src/System/Windows/Forms/Controls/ComboBox/ComboBox.FlatComboAdapter.cs b/src/System.Windows.Forms/src/System/Windows/Forms/Controls/ComboBox/ComboBox.FlatComboAdapter.cs
index 56992511bdb..1823946b07b 100644
--- a/src/System.Windows.Forms/src/System/Windows/Forms/Controls/ComboBox/ComboBox.FlatComboAdapter.cs
+++ b/src/System.Windows.Forms/src/System/Windows/Forms/Controls/ComboBox/ComboBox.FlatComboAdapter.cs
@@ -75,6 +75,11 @@ public virtual void DrawPopUpCombo(ComboBox comboBox, Graphics g)
             {
                 DrawFlatCombo(comboBox, g);
             }
+            else
+            {
+                // Draw the drop down
+                DrawFlatComboDropDown(comboBox, g, _dropDownRect);
+            }
 
             bool rightToLeft = comboBox.RightToLeft == RightToLeft.Yes;
 
diff --git a/src/System.Windows.Forms/src/System/Windows/Forms/Controls/ComboBox/ComboBox.cs b/src/System.Windows.Forms/src/System/Windows/Forms/Controls/ComboBox/ComboBox.cs
index 2ba076ddf47..25227b0bde6 100644
--- a/src/System.Windows.Forms/src/System/Windows/Forms/Controls/ComboBox/ComboBox.cs
+++ b/src/System.Windows.Forms/src/System/Windows/Forms/Controls/ComboBox/ComboBox.cs
@@ -3764,7 +3764,10 @@ protected override unsafe void WndProc(ref Message m)
                     }
 
                     using Graphics g = Graphics.FromHdcInternal((IntPtr)dc);
-                    if ((!Enabled || FlatStyle == FlatStyle.Popup) && MouseIsOver)
+
+                    // The pop up border needs to be drawn only when the control gets the focus or the mouse hovers over it.
+                    bool isPopupAndActive = FlatStyle == FlatStyle.Popup && (Focused || MouseIsOver);
+                    if (!Enabled || isPopupAndActive)
                     {
                         FlatComboBoxAdapter.DrawPopUpCombo(this, g);
                     }
diff --git a/src/System.Windows.Forms/tests/UnitTests/System/Windows/Forms/ComboBoxTests.cs b/src/System.Windows.Forms/tests/UnitTests/System/Windows/Forms/ComboBoxTests.cs
index fbf943b8265..2670358a26d 100644
--- a/src/System.Windows.Forms/tests/UnitTests/System/Windows/Forms/ComboBoxTests.cs
+++ b/src/System.Windows.Forms/tests/UnitTests/System/Windows/Forms/ComboBoxTests.cs
@@ -2750,6 +2750,38 @@ private void InitializeItems(ComboBox comboBox, int numItems)
         Assert.Equal(numItems, comboBox.Items.Count);
     }
 
+    [WinFormsFact]
+    public void ComboBox_OnLostFocus_AutoCompleteModeNone_DoesNotClearMatchingText()
+    {
+        using ComboBox comboBox = new();
+        var comboBoxAccessor = comboBox.TestAccessor().Dynamic;
+        comboBoxAccessor._canFireLostFocus= true;
+        comboBox.AutoCompleteMode = AutoCompleteMode.None;
+        comboBox.AutoCompleteSource = AutoCompleteSource.ListItems;
+        comboBoxAccessor.MatchingText = "Test";
+        comboBox.DropDownStyle = ComboBoxStyle.Simple;
+        comboBoxAccessor.OnLostFocus(EventArgs.Empty);
+
+        string matchingText = comboBoxAccessor.MatchingText;
+        matchingText.Should().Be("Test");
+    }
+
+    [WinFormsFact]
+    public void ComboBox_OnLostFocus_AutoCompleteModeNotNone_ClearsMatchingText()
+    {
+        using ComboBox comboBox = new();
+        var comboBoxAccessor = comboBox.TestAccessor().Dynamic;
+        comboBoxAccessor._canFireLostFocus = true;
+        comboBox.AutoCompleteMode = AutoCompleteMode.Suggest;
+        comboBox.AutoCompleteSource = AutoCompleteSource.ListItems;
+        comboBox.DropDownStyle = ComboBoxStyle.DropDownList;
+        comboBoxAccessor.MatchingText = "Test";
+        comboBoxAccessor.OnLostFocus(EventArgs.Empty);
+
+        string matchingText = comboBoxAccessor.MatchingText;
+        matchingText.Should().BeEmpty();
+    }
+
     private class OwnerDrawComboBox : ComboBox
     {
         public OwnerDrawComboBox()