diff --git a/samples/ControlCatalog/Pages/ComboBoxPage.xaml b/samples/ControlCatalog/Pages/ComboBoxPage.xaml
index eca2c4762c..ab347ac30c 100644
--- a/samples/ControlCatalog/Pages/ComboBoxPage.xaml
+++ b/samples/ControlCatalog/Pages/ComboBoxPage.xaml
@@ -12,8 +12,8 @@
         <StackPanel
             Margin="0,16,0,0"
             HorizontalAlignment="Center"
-            Orientation="Horizontal"
             Spacing="8">
+            <CheckBox IsChecked="{Binding WrapSelection}">WrapSelection</CheckBox>
             <WrapPanel
                 MaxWidth="660"
                 Margin="0,16,0,0"
@@ -99,9 +99,31 @@
                     <ComboBoxItem>Inline Item 4</ComboBoxItem>
                 </ComboBox>
 
-                <ComboBox WrapSelection="{Binding WrapSelection}" ItemsSource="{Binding Values}" DisplayMemberBinding="{Binding Name}">
+                <ComboBox 
+                    WrapSelection="{Binding WrapSelection}" 
+                    ItemsSource="{Binding Values}" 
+                    DisplayMemberBinding="{Binding Name}">
                 
                 </ComboBox>
+              
+                <ComboBox 
+                    WrapSelection="{Binding WrapSelection}" 
+                    PlaceholderText="Different Template"
+                    ItemsSource="{Binding Values}">
+                    <ComboBox.ItemTemplate>
+                        <DataTemplate>
+                            <StackPanel Orientation="Horizontal">
+                                <TextBlock Text="{Binding Name}"></TextBlock>
+                                <TextBlock Text="{Binding Id}"></TextBlock>
+                            </StackPanel>
+                        </DataTemplate>
+                    </ComboBox.ItemTemplate>
+                    <ComboBox.SelectionBoxItemTemplate>
+                        <DataTemplate>
+                            <TextBlock Text="{Binding Name}" Foreground="Red"></TextBlock>
+                        </DataTemplate>
+                    </ComboBox.SelectionBoxItemTemplate>
+                </ComboBox>
 
                 <ComboBox WrapSelection="{Binding WrapSelection}" ItemsSource="{Binding Values}" >
                     <ComboBox.ItemTemplate>
@@ -114,9 +136,6 @@
                     </ComboBox.ItemTemplate>
                 </ComboBox>
             </WrapPanel>
-
-            <CheckBox IsChecked="{Binding WrapSelection}">WrapSelection</CheckBox>
-
         </StackPanel>
     </StackPanel>
 </UserControl>
diff --git a/src/Avalonia.Controls/ComboBox.cs b/src/Avalonia.Controls/ComboBox.cs
index 78bb191e93..f1cc84f7a4 100644
--- a/src/Avalonia.Controls/ComboBox.cs
+++ b/src/Avalonia.Controls/ComboBox.cs
@@ -5,10 +5,12 @@ using Avalonia.Controls.Metadata;
 using Avalonia.Controls.Primitives;
 using Avalonia.Controls.Shapes;
 using Avalonia.Controls.Templates;
+using Avalonia.Data;
 using Avalonia.Input;
 using Avalonia.Interactivity;
 using Avalonia.Layout;
 using Avalonia.Media;
+using Avalonia.Metadata;
 using Avalonia.Reactive;
 using Avalonia.VisualTree;
 
@@ -71,6 +73,23 @@ namespace Avalonia.Controls
         /// </summary>
         public static readonly StyledProperty<VerticalAlignment> VerticalContentAlignmentProperty =
             ContentControl.VerticalContentAlignmentProperty.AddOwner<ComboBox>();
+        
+        /// <summary>
+        /// Defines the <see cref="SelectionBoxItemTemplate"/> property.
+        /// </summary>
+        public static readonly StyledProperty<IDataTemplate?> SelectionBoxItemTemplateProperty =
+            AvaloniaProperty.Register<ComboBox, IDataTemplate?>(
+                nameof(SelectionBoxItemTemplate), defaultBindingMode: BindingMode.TwoWay, coerce: CoerceSelectionBoxItemTemplate);
+        
+        private static IDataTemplate? CoerceSelectionBoxItemTemplate(AvaloniaObject obj, IDataTemplate? template)
+        {
+            if (template is not null) return template;
+            if(obj is ComboBox comboBox && template is null)
+            {
+                return comboBox.ItemTemplate;
+            }
+            return template;
+        }
 
         private Popup? _popup;
         private object? _selectionBoxItem;
@@ -159,6 +178,16 @@ namespace Avalonia.Controls
             set => SetValue(VerticalContentAlignmentProperty, value);
         }
 
+        /// <summary>
+        /// Gets or sets the DataTemplate used to display the selected item. This has a higher priority than <see cref="ItemsControl.ItemTemplate"/> if set.
+        /// </summary>
+        [InheritDataTypeFromItems(nameof(ItemsSource))]
+        public IDataTemplate? SelectionBoxItemTemplate
+        {
+            get => GetValue(SelectionBoxItemTemplateProperty);
+            set => SetValue(SelectionBoxItemTemplateProperty, value);
+        }
+
         protected override void OnAttachedToVisualTree(VisualTreeAttachmentEventArgs e)
         {
             base.OnAttachedToVisualTree(e);
@@ -322,7 +351,10 @@ namespace Avalonia.Controls
             {
                 PseudoClasses.Set(pcDropdownOpen, change.GetNewValue<bool>());
             }
-
+            else if (change.Property == ItemTemplateProperty)
+            {
+                CoerceValue(SelectionBoxItemTemplateProperty);
+            }
             base.OnPropertyChanged(change);
         }
 
@@ -433,7 +465,7 @@ namespace Avalonia.Controls
             }
             else
             {
-                if(ItemTemplate is null && DisplayMemberBinding is { } binding)
+                if(ItemTemplate is null && SelectionBoxItemTemplate is null && DisplayMemberBinding is { } binding)
                 {
                     var template = new FuncDataTemplate<object?>((_, _) =>
                     new TextBlock
diff --git a/src/Avalonia.Themes.Fluent/Controls/ComboBox.xaml b/src/Avalonia.Themes.Fluent/Controls/ComboBox.xaml
index 5efe6f1790..d3c8417875 100644
--- a/src/Avalonia.Themes.Fluent/Controls/ComboBox.xaml
+++ b/src/Avalonia.Themes.Fluent/Controls/ComboBox.xaml
@@ -84,11 +84,12 @@
                        IsVisible="{TemplateBinding SelectionBoxItem, Converter={x:Static ObjectConverters.IsNull}}" />
             <ContentControl x:Name="ContentPresenter"
                             Content="{TemplateBinding SelectionBoxItem}"
-                            ContentTemplate="{TemplateBinding ItemTemplate}"
                             Grid.Column="0"
                             Margin="{TemplateBinding Padding}"
                             HorizontalContentAlignment="{TemplateBinding HorizontalContentAlignment}"
-                            VerticalContentAlignment="{TemplateBinding VerticalContentAlignment}" />
+                            ContentTemplate="{TemplateBinding SelectionBoxItemTemplate}"
+                            VerticalContentAlignment="{TemplateBinding VerticalContentAlignment}">
+            </ContentControl>
 
             <Border x:Name="DropDownOverlay"
                     Grid.Column="1"
diff --git a/src/Avalonia.Themes.Simple/Controls/ComboBox.xaml b/src/Avalonia.Themes.Simple/Controls/ComboBox.xaml
index 910d8fba68..cbb40d7ff3 100644
--- a/src/Avalonia.Themes.Simple/Controls/ComboBox.xaml
+++ b/src/Avalonia.Themes.Simple/Controls/ComboBox.xaml
@@ -34,7 +34,8 @@
                             HorizontalContentAlignment="{TemplateBinding HorizontalContentAlignment}"
                             VerticalContentAlignment="{TemplateBinding VerticalContentAlignment}"
                             Content="{TemplateBinding SelectionBoxItem}"
-                            ContentTemplate="{TemplateBinding ItemTemplate}" />
+                            ContentTemplate="{TemplateBinding SelectionBoxItemTemplate}">
+            </ContentControl>
             <ToggleButton Name="toggle"
                           Grid.Column="1"
                           Background="Transparent"
diff --git a/tests/Avalonia.Controls.UnitTests/ComboBoxTests.cs b/tests/Avalonia.Controls.UnitTests/ComboBoxTests.cs
index 3de13ba71b..162e3a6f8e 100644
--- a/tests/Avalonia.Controls.UnitTests/ComboBoxTests.cs
+++ b/tests/Avalonia.Controls.UnitTests/ComboBoxTests.cs
@@ -453,5 +453,69 @@ namespace Avalonia.Controls.UnitTests
                 Assert.Equal(FlowDirection.RightToLeft, rectangle.FlowDirection);
             }
         }
+
+        [Fact]
+        public void SelectionBoxItemTemplate_Overrides_ItemTemplate()
+        {
+            IDataTemplate itemTemplate = new FuncDataTemplate<string>((x, _) => new TextBlock { Text = x + "!" });
+            IDataTemplate selectionBoxItemTemplate = new FuncDataTemplate<string>((x, _) => new TextBlock { Text = x });
+            var target = new ComboBox
+            {
+                ItemsSource = new []{ "Foo" },
+                SelectionBoxItemTemplate = selectionBoxItemTemplate,
+                ItemTemplate = itemTemplate,
+            };
+            
+            Assert.Equal(selectionBoxItemTemplate, target.SelectionBoxItemTemplate);
+        }
+        
+        [Fact]
+        public void SelectionBoxItemTemplate_Inherits_From_ItemTemplate_When_NotSet()
+        {
+            IDataTemplate itemTemplate = new FuncDataTemplate<string>((x, _) => new TextBlock { Text = x + "!" });
+            var target = new ComboBox
+            {
+                ItemsSource = new []{ "Foo" },
+                ItemTemplate = itemTemplate,
+            };
+            
+            Assert.Equal(itemTemplate, target.SelectionBoxItemTemplate);
+        }
+
+        [Fact]
+        public void SelectionBoxItemTemplate_Overrides_ItemTemplate_After_ItemTemplate_Changed()
+        {
+            IDataTemplate itemTemplate = new FuncDataTemplate<string>((x, _) => new TextBlock { Text = x + "!" });
+            IDataTemplate selectionBoxItemTemplate = new FuncDataTemplate<string>((x, _) => new TextBlock { Text = x });
+            IDataTemplate itemTemplate2 = new FuncDataTemplate<string>((x, _) => new TextBlock { Text = x + "?" });
+            var target = new ComboBox
+            {
+                ItemsSource = new[] { "Foo" },
+                SelectionBoxItemTemplate = selectionBoxItemTemplate,
+                ItemTemplate = itemTemplate,
+            };
+
+            Assert.Equal(selectionBoxItemTemplate, target.SelectionBoxItemTemplate);
+            
+            target.ItemTemplate = itemTemplate2;
+            
+            Assert.Equal(selectionBoxItemTemplate, target.SelectionBoxItemTemplate);
+        }
+
+        [Fact]
+        public void SelectionBoxItemTemplate_Inherits_From_ItemTemplate_When_ItemTemplate_Changed()
+        {
+            IDataTemplate itemTemplate = new FuncDataTemplate<string>((x, _) => new TextBlock { Text = x + "!" });
+            IDataTemplate selectionBoxItemTemplate = new FuncDataTemplate<string>((x, _) => new TextBlock { Text = x });
+            IDataTemplate itemTemplate2 = new FuncDataTemplate<string>((x, _) => new TextBlock { Text = x + "?" });
+            var target = new ComboBox { ItemsSource = new[] { "Foo" }, ItemTemplate = itemTemplate, };
+
+            Assert.Equal(itemTemplate, target.SelectionBoxItemTemplate);
+
+            target.ItemTemplate = itemTemplate2;
+            target.SelectionBoxItemTemplate = null;
+
+            Assert.Equal(itemTemplate2, target.SelectionBoxItemTemplate);
+        }
     }
 }