diff --git a/src/Avalonia.Controls/ComboBox.cs b/src/Avalonia.Controls/ComboBox.cs
index dbdbf4b536..e34f9d2613 100644
--- a/src/Avalonia.Controls/ComboBox.cs
+++ b/src/Avalonia.Controls/ComboBox.cs
@@ -471,7 +471,7 @@ namespace Avalonia.Controls
             }
             else
             {
-                if(ItemTemplate is null && SelectionBoxItemTemplate is null && DisplayMemberBinding is { } binding)
+                if (item is not null && ItemTemplate is null && SelectionBoxItemTemplate is null && DisplayMemberBinding is { } binding)
                 {
                     var template = new FuncDataTemplate<object?>((_, _) =>
                     new TextBlock
diff --git a/tests/Avalonia.Controls.UnitTests/ComboBoxTests.cs b/tests/Avalonia.Controls.UnitTests/ComboBoxTests.cs
index 65243fa445..22cafb403b 100644
--- a/tests/Avalonia.Controls.UnitTests/ComboBoxTests.cs
+++ b/tests/Avalonia.Controls.UnitTests/ComboBoxTests.cs
@@ -517,5 +517,24 @@ namespace Avalonia.Controls.UnitTests
 
             Assert.Equal(itemTemplate2, target.SelectionBoxItemTemplate);
         }
+
+        [Fact]
+        public void DisplayMemberBinding_Is_Not_Applied_To_SelectionBoxItem_Without_Selection()
+        {
+            var target = new ComboBox
+            {
+                DisplayMemberBinding = new Binding(),
+                ItemsSource = new[] { "foo", "bar" }
+            };
+
+            target.SelectedItem = null;
+            Assert.Null(target.SelectionBoxItem);
+
+            target.SelectedItem = "foo";
+            Assert.NotNull(target.SelectionBoxItem);
+
+            target.SelectedItem = null;
+            Assert.Null(target.SelectionBoxItem);
+        }
     }
 }