diff --git a/src/Avalonia.Controls/ToolTip.cs b/src/Avalonia.Controls/ToolTip.cs
index 060d559d1a..cff3dab150 100644
--- a/src/Avalonia.Controls/ToolTip.cs
+++ b/src/Avalonia.Controls/ToolTip.cs
@@ -105,20 +105,17 @@ namespace Avalonia.Controls
         {
             if (control != null && control.IsVisible && control.GetVisualRoot() != null)
             {
-                if (s_popup == null)
+                if (s_popup != null)
                 {
-                    s_popup = new PopupRoot
-                    {
-                        Content = new ToolTip(),
-                    };
-
-                    ((ISetLogicalParent)s_popup).SetParent(control);
+                    throw new AvaloniaInternalException("Previous ToolTip not disposed.");
                 }
 
                 var cp = MouseDevice.Instance?.GetPosition(control);
                 var position = control.PointToScreen(cp ?? new Point(0, 0)) + new Vector(0, 22);
 
-                ((ToolTip)s_popup.Content).Content = GetTip(control);
+                s_popup = new PopupRoot();
+                ((ISetLogicalParent)s_popup).SetParent(control);
+                s_popup.Content = new ToolTip { Content = GetTip(control) };
                 s_popup.Position = position;
                 s_popup.Show();
 
@@ -148,9 +145,15 @@ namespace Avalonia.Controls
 
             if (control == s_current)
             {
-                if (s_popup != null && s_popup.IsVisible)
+                if (s_popup != null)
                 {
-                    s_popup.Hide();
+                    // Clear the ToolTip's Content in case it has control content: this will
+                    // reset its visual parent allowing it to be used again.
+                    ((ToolTip)s_popup.Content).Content = null;
+
+                    // Dispose of the popup.
+                    s_popup.Dispose();
+                    s_popup = null;
                 }
 
                 s_show.OnNext(null);
diff --git a/src/Avalonia.Themes.Default/Accents/BaseLight.xaml b/src/Avalonia.Themes.Default/Accents/BaseLight.xaml
index 0dae3e1a21..38786f54d3 100644
--- a/src/Avalonia.Themes.Default/Accents/BaseLight.xaml
+++ b/src/Avalonia.Themes.Default/Accents/BaseLight.xaml
@@ -19,6 +19,7 @@
     <SolidColorBrush x:Key="ThemeAccentBrush3">#66119EDA</SolidColorBrush>
     <SolidColorBrush x:Key="ThemeAccentBrush4">#33119EDA</SolidColorBrush>
     <SolidColorBrush x:Key="ErrorBrush">Red</SolidColorBrush>
+    <SolidColorBrush x:Key="ErrorBrushLight">#10ff0000</SolidColorBrush>
 
     <sys:Double x:Key="ThemeBorderThickness">2</sys:Double>
     <sys:Double x:Key="ThemeDisabledOpacity">0.5</sys:Double>
diff --git a/src/Avalonia.Themes.Default/DefaultTheme.xaml b/src/Avalonia.Themes.Default/DefaultTheme.xaml
index 0fab9ceec7..026834e808 100644
--- a/src/Avalonia.Themes.Default/DefaultTheme.xaml
+++ b/src/Avalonia.Themes.Default/DefaultTheme.xaml
@@ -1,4 +1,7 @@
 <Styles xmlns="https://github.com/avaloniaui">
+  <!-- Define ToolTip first so its styles can be overriden by other controls (e.g. TextBox) -->
+  <StyleInclude Source="resm:Avalonia.Themes.Default.ToolTip.xaml?assembly=Avalonia.Themes.Default"/>
+
   <StyleInclude Source="resm:Avalonia.Themes.Default.FocusAdorner.xaml?assembly=Avalonia.Themes.Default"/>
   <StyleInclude Source="resm:Avalonia.Themes.Default.Button.xaml?assembly=Avalonia.Themes.Default"/>
   <StyleInclude Source="resm:Avalonia.Themes.Default.Carousel.xaml?assembly=Avalonia.Themes.Default"/>
@@ -28,7 +31,6 @@
   <StyleInclude Source="resm:Avalonia.Themes.Default.TextBox.xaml?assembly=Avalonia.Themes.Default"/>
   <StyleInclude Source="resm:Avalonia.Themes.Default.ToggleButton.xaml?assembly=Avalonia.Themes.Default"/>
   <StyleInclude Source="resm:Avalonia.Themes.Default.Expander.xaml?assembly=Avalonia.Themes.Default"/>
-  <StyleInclude Source="resm:Avalonia.Themes.Default.ToolTip.xaml?assembly=Avalonia.Themes.Default"/>
   <StyleInclude Source="resm:Avalonia.Themes.Default.TreeView.xaml?assembly=Avalonia.Themes.Default"/>
   <StyleInclude Source="resm:Avalonia.Themes.Default.TreeViewItem.xaml?assembly=Avalonia.Themes.Default"/>
   <StyleInclude Source="resm:Avalonia.Themes.Default.Window.xaml?assembly=Avalonia.Themes.Default"/>
diff --git a/src/Avalonia.Themes.Default/TextBox.xaml b/src/Avalonia.Themes.Default/TextBox.xaml
index 89297d2446..a41f40cc5f 100644
--- a/src/Avalonia.Themes.Default/TextBox.xaml
+++ b/src/Avalonia.Themes.Default/TextBox.xaml
@@ -78,6 +78,7 @@
     <Setter Property="IsVisible" Value="True"/>
   </Style>
   <Style Selector="TextBox /template/ ToolTip">
-    <Setter Property="BorderBrush" Value="Red"/>
+    <Setter Property="Background" Value="{StyleResource ErrorBrushLight}"/>
+    <Setter Property="BorderBrush" Value="{StyleResource ErrorBrush}"/>
   </Style>
 </Styles>
\ No newline at end of file