diff --git a/src/Avalonia.Base/Styling/ChildSelector.cs b/src/Avalonia.Base/Styling/ChildSelector.cs
index 34f3a76b61..9512dc34df 100644
--- a/src/Avalonia.Base/Styling/ChildSelector.cs
+++ b/src/Avalonia.Base/Styling/ChildSelector.cs
@@ -65,6 +65,6 @@ namespace Avalonia.Styling
         }
 
         protected override Selector? MovePrevious() => null;
-        internal override bool HasValidNestingSelector() => _parent.HasValidNestingSelector();
+        protected override Selector? MovePreviousOrParent() => _parent;
     }
 }
diff --git a/src/Avalonia.Base/Styling/DescendentSelector.cs b/src/Avalonia.Base/Styling/DescendentSelector.cs
index 4ffaff6861..677a924189 100644
--- a/src/Avalonia.Base/Styling/DescendentSelector.cs
+++ b/src/Avalonia.Base/Styling/DescendentSelector.cs
@@ -70,6 +70,6 @@ namespace Avalonia.Styling
         }
 
         protected override Selector? MovePrevious() => null;
-        internal override bool HasValidNestingSelector() => _parent.HasValidNestingSelector();
+        protected override Selector? MovePreviousOrParent() => _parent;
     }
 }
diff --git a/src/Avalonia.Base/Styling/NestingSelector.cs b/src/Avalonia.Base/Styling/NestingSelector.cs
index 4393d3239f..77c5b719c6 100644
--- a/src/Avalonia.Base/Styling/NestingSelector.cs
+++ b/src/Avalonia.Base/Styling/NestingSelector.cs
@@ -33,6 +33,6 @@ namespace Avalonia.Styling
         }
 
         protected override Selector? MovePrevious() => null;
-        internal override bool HasValidNestingSelector() => true;
+        protected override Selector? MovePreviousOrParent() => null;
     }
 }
diff --git a/src/Avalonia.Base/Styling/NotSelector.cs b/src/Avalonia.Base/Styling/NotSelector.cs
index 76a0690e96..c7727bb6b8 100644
--- a/src/Avalonia.Base/Styling/NotSelector.cs
+++ b/src/Avalonia.Base/Styling/NotSelector.cs
@@ -67,6 +67,6 @@ namespace Avalonia.Styling
         }
 
         protected override Selector? MovePrevious() => _previous;
-        internal override bool HasValidNestingSelector() => _previous?.HasValidNestingSelector() ?? false;
+        protected override Selector? MovePreviousOrParent() => _previous;
     }
 }
diff --git a/src/Avalonia.Base/Styling/NthChildSelector.cs b/src/Avalonia.Base/Styling/NthChildSelector.cs
index 047bf434da..f473791664 100644
--- a/src/Avalonia.Base/Styling/NthChildSelector.cs
+++ b/src/Avalonia.Base/Styling/NthChildSelector.cs
@@ -105,7 +105,7 @@ namespace Avalonia.Styling
         }
 
         protected override Selector? MovePrevious() => _previous;
-        internal override bool HasValidNestingSelector() => _previous?.HasValidNestingSelector() ?? false;
+        protected override Selector? MovePreviousOrParent() => _previous;
 
         public override string ToString()
         {
diff --git a/src/Avalonia.Base/Styling/OrSelector.cs b/src/Avalonia.Base/Styling/OrSelector.cs
index 913c27bf0c..af9249864f 100644
--- a/src/Avalonia.Base/Styling/OrSelector.cs
+++ b/src/Avalonia.Base/Styling/OrSelector.cs
@@ -103,18 +103,12 @@ namespace Avalonia.Styling
         }
 
         protected override Selector? MovePrevious() => null;
+        protected override Selector? MovePreviousOrParent() => null;
 
-        internal override bool HasValidNestingSelector()
+        internal override void ValidateNestingSelector(bool inControlTheme)
         {
             foreach (var selector in _selectors)
-            {
-                if (!selector.HasValidNestingSelector())
-                {
-                    return false;
-                }
-            }
-
-            return true;
+                selector.ValidateNestingSelector(inControlTheme);
         }
 
         private Type? EvaluateTargetType()
diff --git a/src/Avalonia.Base/Styling/PropertyEqualsSelector.cs b/src/Avalonia.Base/Styling/PropertyEqualsSelector.cs
index 7a37daf087..48136ba2de 100644
--- a/src/Avalonia.Base/Styling/PropertyEqualsSelector.cs
+++ b/src/Avalonia.Base/Styling/PropertyEqualsSelector.cs
@@ -90,7 +90,7 @@ namespace Avalonia.Styling
         }
 
         protected override Selector? MovePrevious() => _previous;
-        internal override bool HasValidNestingSelector() => _previous?.HasValidNestingSelector() ?? false;
+        protected override Selector? MovePreviousOrParent() => _previous;
 
         internal static bool Compare(Type propertyType, object? propertyValue, object? value)
         {
diff --git a/src/Avalonia.Base/Styling/Selector.cs b/src/Avalonia.Base/Styling/Selector.cs
index 1e06f3d375..7ce17518dd 100644
--- a/src/Avalonia.Base/Styling/Selector.cs
+++ b/src/Avalonia.Base/Styling/Selector.cs
@@ -86,7 +86,36 @@ namespace Avalonia.Styling
         /// </summary>
         protected abstract Selector? MovePrevious();
 
-        internal abstract bool HasValidNestingSelector();
+        /// <summary>
+        /// Moves to the previous selector or the parent selector.
+        /// </summary>
+        protected abstract Selector? MovePreviousOrParent();
+
+        internal virtual void ValidateNestingSelector(bool inControlTheme)
+        {
+            var s = this;
+            var templateCount = 0;
+
+            do
+            {
+                if (inControlTheme)
+                {
+                    if (!s.InTemplate && s.IsCombinator)
+                        throw new InvalidOperationException(
+                            "ControlTheme style may not directly contain a child or descendent selector.");
+                    if (s is TemplateSelector && templateCount++ > 0)
+                        throw new InvalidOperationException(
+                            "ControlTemplate styles cannot contain multiple template selectors.");
+                }
+
+                var previous = s.MovePreviousOrParent();
+
+                if (previous is null && s is not NestingSelector)
+                    throw new InvalidOperationException("Child styles must have a nesting selector.");
+
+                s = previous;
+            } while (s is not null);
+        }
 
         private static SelectorMatch MatchUntilCombinator(
             IStyleable control,
diff --git a/src/Avalonia.Base/Styling/Style.cs b/src/Avalonia.Base/Styling/Style.cs
index 7a6b746488..77c4e62d29 100644
--- a/src/Avalonia.Base/Styling/Style.cs
+++ b/src/Avalonia.Base/Styling/Style.cs
@@ -77,8 +77,13 @@ namespace Avalonia.Styling
             {
                 if (Selector is null)
                     throw new InvalidOperationException("Child styles must have a selector.");
-                if (!Selector.HasValidNestingSelector())
-                    throw new InvalidOperationException("Child styles must have a nesting selector.");
+                Selector.ValidateNestingSelector(false);
+            }
+            else if (parent is ControlTheme)
+            {
+                if (Selector is null)
+                    throw new InvalidOperationException("Child styles must have a selector.");
+                Selector.ValidateNestingSelector(true);
             }
 
             base.SetParent(parent);
diff --git a/src/Avalonia.Base/Styling/Styles.cs b/src/Avalonia.Base/Styling/Styles.cs
index 4c011f1b0d..3a27275438 100644
--- a/src/Avalonia.Base/Styling/Styles.cs
+++ b/src/Avalonia.Base/Styling/Styles.cs
@@ -26,6 +26,11 @@ namespace Avalonia.Styling
         {
             _styles.ResetBehavior = ResetBehavior.Remove;
             _styles.CollectionChanged += OnCollectionChanged;
+            _styles.Validate = i =>
+            {
+                if (i is ControlTheme)
+                    throw new InvalidOperationException("ControlThemes cannot be added to a Styles collection.");
+            };
         }
 
         public Styles(IResourceHost owner)
diff --git a/src/Avalonia.Base/Styling/TemplateSelector.cs b/src/Avalonia.Base/Styling/TemplateSelector.cs
index b0a2dae8d6..278e24a203 100644
--- a/src/Avalonia.Base/Styling/TemplateSelector.cs
+++ b/src/Avalonia.Base/Styling/TemplateSelector.cs
@@ -49,6 +49,6 @@ namespace Avalonia.Styling
         }
 
         protected override Selector? MovePrevious() => null;
-        internal override bool HasValidNestingSelector() => _parent?.HasValidNestingSelector() ?? false;
+        protected override Selector? MovePreviousOrParent() => _parent;
     }
 }
diff --git a/src/Avalonia.Base/Styling/TypeNameAndClassSelector.cs b/src/Avalonia.Base/Styling/TypeNameAndClassSelector.cs
index 24d5d6bbbf..6681a7da36 100644
--- a/src/Avalonia.Base/Styling/TypeNameAndClassSelector.cs
+++ b/src/Avalonia.Base/Styling/TypeNameAndClassSelector.cs
@@ -140,7 +140,7 @@ namespace Avalonia.Styling
         }
 
         protected override Selector? MovePrevious() => _previous;
-        internal override bool HasValidNestingSelector() => _previous?.HasValidNestingSelector() ?? false;
+        protected override Selector? MovePreviousOrParent() => _previous;
 
         private string BuildSelectorString()
         {
diff --git a/tests/Avalonia.Base.UnitTests/Styling/ControlThemeTests.cs b/tests/Avalonia.Base.UnitTests/Styling/ControlThemeTests.cs
index 93a0e6c2fd..7a27a02fc4 100644
--- a/tests/Avalonia.Base.UnitTests/Styling/ControlThemeTests.cs
+++ b/tests/Avalonia.Base.UnitTests/Styling/ControlThemeTests.cs
@@ -1,5 +1,6 @@
 using System;
 using Avalonia.Controls;
+using Avalonia.Controls.Primitives;
 using Avalonia.Styling;
 using Xunit;
 
@@ -7,6 +8,15 @@ namespace Avalonia.Base.UnitTests.Styling
 {
     public class ControlThemeTests
     {
+        [Fact]
+        public void ControlTheme_Cannot_Be_Added_To_Styles()
+        {
+            var target = new ControlTheme(typeof(Button));
+            var styles = new Styles();
+
+            Assert.Throws<InvalidOperationException>(() => styles.Add(target));
+        }
+
         [Fact]
         public void ControlTheme_Cannot_Be_Added_To_Style_Children()
         {
@@ -24,5 +34,59 @@ namespace Avalonia.Base.UnitTests.Styling
 
             Assert.Throws<InvalidOperationException>(() => other.Children.Add(target));
         }
+
+        [Fact]
+        public void Style_Without_Selector_Cannot_Be_Added_To_Children()
+        {
+            var target = new ControlTheme(typeof(Button));
+            var child = new Style();
+
+            Assert.Throws<InvalidOperationException>(() => target.Children.Add(child));
+        }
+
+        [Fact]
+        public void Style_Without_Nesting_Selector_Cannot_Be_Added_To_Children()
+        {
+            var target = new ControlTheme(typeof(Button));
+            var child = new Style(x => x.OfType<Button>().Template().OfType<Border>());
+
+            Assert.Throws<InvalidOperationException>(() => target.Children.Add(child));
+        }
+
+        [Fact]
+        public void Style_With_NonTemplate_Child_Selector_Cannot_Be_Added_To_Children()
+        {
+            var target = new ControlTheme(typeof(Button));
+            var child = new Style(x => x.Nesting().Child().OfType<Border>());
+
+            Assert.Throws<InvalidOperationException>(() => target.Children.Add(child));
+        }
+
+        [Fact]
+        public void Style_With_NonTemplate_Descendent_Selector_Cannot_Be_Added_To_Children()
+        {
+            var target = new ControlTheme(typeof(Button));
+            var child = new Style(x => x.Nesting().Descendant().OfType<Border>());
+
+            Assert.Throws<InvalidOperationException>(() => target.Children.Add(child));
+        }
+
+        [Fact]
+        public void Style_With_NonTemplate_Child_Template_Selector_Cannot_Be_Added_To_Children()
+        {
+            var target = new ControlTheme(typeof(Button));
+            var child = new Style(x => x.Nesting().Child().Template().OfType<Border>());
+
+            Assert.Throws<InvalidOperationException>(() => target.Children.Add(child));
+        }
+
+        [Fact]
+        public void Style_With_Double_Template_Selector_Cannot_Be_Added_To_Children()
+        {
+            var target = new ControlTheme(typeof(Button));
+            var child = new Style(x => x.Nesting().Template().OfType<ToggleButton>().Template().OfType<Border>());
+
+            Assert.Throws<InvalidOperationException>(() => target.Children.Add(child));
+        }
     }
 }