diff --git a/src/Markup/Avalonia.Markup.Xaml/Templates/DataTemplate.cs b/src/Markup/Avalonia.Markup.Xaml/Templates/DataTemplate.cs
index 07c5451135..650534b347 100644
--- a/src/Markup/Avalonia.Markup.Xaml/Templates/DataTemplate.cs
+++ b/src/Markup/Avalonia.Markup.Xaml/Templates/DataTemplate.cs
@@ -30,7 +30,7 @@ namespace Avalonia.Markup.Xaml.Templates
 
         public IControl Build(object data, IControl existing)
         {
-            return existing ?? TemplateContent.Load(Content).Control;
+            return existing ?? TemplateContent.Load(Content)?.Control;
         }
     }
 }
diff --git a/src/Markup/Avalonia.Markup.Xaml/Templates/ItemsPanelTemplate.cs b/src/Markup/Avalonia.Markup.Xaml/Templates/ItemsPanelTemplate.cs
index c8843a3176..c096ed7ed7 100644
--- a/src/Markup/Avalonia.Markup.Xaml/Templates/ItemsPanelTemplate.cs
+++ b/src/Markup/Avalonia.Markup.Xaml/Templates/ItemsPanelTemplate.cs
@@ -10,8 +10,7 @@ namespace Avalonia.Markup.Xaml.Templates
         [TemplateContent]
         public object Content { get; set; }
 
-        public IPanel Build()
-                => (IPanel)TemplateContent.Load(Content).Control;
+        public IPanel Build() => (IPanel)TemplateContent.Load(Content)?.Control;
 
         object ITemplate.Build() => Build();
     }
diff --git a/src/Markup/Avalonia.Markup.Xaml/Templates/Template.cs b/src/Markup/Avalonia.Markup.Xaml/Templates/Template.cs
index 65323ae665..45fae9cb28 100644
--- a/src/Markup/Avalonia.Markup.Xaml/Templates/Template.cs
+++ b/src/Markup/Avalonia.Markup.Xaml/Templates/Template.cs
@@ -10,7 +10,7 @@ namespace Avalonia.Markup.Xaml.Templates
         [TemplateContent]
         public object Content { get; set; }
 
-        public IControl Build() => TemplateContent.Load(Content).Control;
+        public IControl Build() => TemplateContent.Load(Content)?.Control;
 
         object ITemplate.Build() => Build();
     }
diff --git a/src/Markup/Avalonia.Markup.Xaml/Templates/TemplateContent.cs b/src/Markup/Avalonia.Markup.Xaml/Templates/TemplateContent.cs
index 96f25668fb..483a1a5d06 100644
--- a/src/Markup/Avalonia.Markup.Xaml/Templates/TemplateContent.cs
+++ b/src/Markup/Avalonia.Markup.Xaml/Templates/TemplateContent.cs
@@ -1,6 +1,4 @@
 using System;
-using Avalonia.Controls;
-using System.Collections.Generic;
 using Avalonia.Controls.Templates;
 
 namespace Avalonia.Markup.Xaml.Templates
@@ -14,6 +12,12 @@ namespace Avalonia.Markup.Xaml.Templates
             {
                 return (ControlTemplateResult)direct(null);
             }
+
+            if (templateContent is null)
+            {
+                return null;
+            }
+
             throw new ArgumentException(nameof(templateContent));
         }
     }
diff --git a/src/Markup/Avalonia.Markup.Xaml/Templates/TreeDataTemplate.cs b/src/Markup/Avalonia.Markup.Xaml/Templates/TreeDataTemplate.cs
index d785ac4ac0..7b065c7f47 100644
--- a/src/Markup/Avalonia.Markup.Xaml/Templates/TreeDataTemplate.cs
+++ b/src/Markup/Avalonia.Markup.Xaml/Templates/TreeDataTemplate.cs
@@ -51,8 +51,12 @@ namespace Avalonia.Markup.Xaml.Templates
 
         public IControl Build(object data)
         {
-            var visualTreeForItem = TemplateContent.Load(Content).Control;
-            visualTreeForItem.DataContext = data;
+            var visualTreeForItem = TemplateContent.Load(Content)?.Control;
+            if (visualTreeForItem != null)
+            {
+                visualTreeForItem.DataContext = data;
+            }
+
             return visualTreeForItem;
         }
     }
diff --git a/tests/Avalonia.Markup.Xaml.UnitTests/Xaml/DataTemplateTests.cs b/tests/Avalonia.Markup.Xaml.UnitTests/Xaml/DataTemplateTests.cs
index 033b670bf4..53881467e7 100644
--- a/tests/Avalonia.Markup.Xaml.UnitTests/Xaml/DataTemplateTests.cs
+++ b/tests/Avalonia.Markup.Xaml.UnitTests/Xaml/DataTemplateTests.cs
@@ -7,6 +7,31 @@ namespace Avalonia.Markup.Xaml.UnitTests.Xaml
 {
     public class DataTemplateTests : XamlTestBase
     {
+        [Fact]
+        public void DataTemplate_Can_Be_Empty()
+        {
+            using (UnitTestApplication.Start(TestServices.StyledWindow))
+            {
+                var xaml = @"
+<Window xmlns='https://github.com/avaloniaui'
+        xmlns:sys='clr-namespace:System;assembly=netstandard'
+        xmlns:x='http://schemas.microsoft.com/winfx/2006/xaml'>
+    <Window.DataTemplates>
+        <DataTemplate DataType='{x:Type sys:String}' />
+    </Window.DataTemplates>
+    <ContentControl Name='target' Content='Foo'/>
+</Window>";
+                var window = (Window)AvaloniaRuntimeXamlLoader.Load(xaml);
+                var target = window.FindControl<ContentControl>("target");
+
+                window.ApplyTemplate();
+                target.ApplyTemplate();
+                ((ContentPresenter)target.Presenter).UpdateChild();
+
+                Assert.Null(target.Presenter.Child);
+            }
+        }
+
         [Fact]
         public void DataTemplate_Can_Contain_Name()
         {