diff --git a/ILSpy.Tests/Editor/MarginCursorTests.cs b/ILSpy.Tests/Editor/MarginCursorTests.cs
index 786898286..6ecec59ab 100644
--- a/ILSpy.Tests/Editor/MarginCursorTests.cs
+++ b/ILSpy.Tests/Editor/MarginCursorTests.cs
@@ -17,9 +17,11 @@
 // DEALINGS IN THE SOFTWARE.
 
 using System.Linq;
+using System.Reflection;
 using System.Threading.Tasks;
 
 using Avalonia.Controls;
+using Avalonia.Headless;
 using Avalonia.Headless.NUnit;
 
 using AvaloniaEdit.Editing;
@@ -75,4 +77,37 @@ public class MarginCursorTests
 				$"the {margin.GetType().Name} is a click target, so it must show the arrow rather than the text I-beam");
 		}
 	}
+
+	[AvaloniaTest]
+	public async Task Toggling_Line_Numbers_On_Live_Keeps_Gutter_Order_And_Positive_Font_Size()
+	{
+		var (window, vm) = await TestHarness.BootAsync(1);
+		var settings = AppComposition.Current.GetExport<SettingsService>().DisplaySettings;
+		settings.ShowLineNumbers = false;
+
+		var coreLibName = typeof(object).Assembly.GetName().Name!;
+		var objectNode = vm.AssemblyTreeModel.FindNode<TypeTreeNode>(coreLibName, "System", "System.Object");
+		vm.AssemblyTreeModel.SelectNode(objectNode);
+		await vm.DockWorkspace.WaitForDecompiledTextAsync();
+		var view = await window.WaitForComponent<DecompilerTextView>();
+
+		settings.ShowLineNumbers = true;
+		var margins = view.Editor.TextArea.LeftMargins;
+		var lineNumberMargin = margins.OfType<LineNumberMargin>()
+			.Should().ContainSingle("line numbers should render after being toggled on live").Which;
+		margins.IndexOf(margins.OfType<BookmarkMargin>().Single())
+			.Should().Be(margins.IndexOf(lineNumberMargin) - 1,
+				"the bookmark gutter must stay left of line numbers when line numbers are toggled on live");
+		GetLineNumberMarginEmSize(lineNumberMargin).Should().BeGreaterThan(0);
+
+		window.UpdateLayout();
+		AvaloniaHeadlessPlatform.ForceRenderTimerTick();
+	}
+
+	static double GetLineNumberMarginEmSize(LineNumberMargin margin)
+	{
+		return (double)typeof(LineNumberMargin)
+			.GetProperty("EmSize", BindingFlags.Instance | BindingFlags.NonPublic)!
+			.GetValue(margin)!;
+	}
 }
diff --git a/ILSpy/TextView/DecompilerTextEditor.cs b/ILSpy/TextView/DecompilerTextEditor.cs
index 8df849bc0..d6c6ce057 100644
--- a/ILSpy/TextView/DecompilerTextEditor.cs
+++ b/ILSpy/TextView/DecompilerTextEditor.cs
@@ -18,6 +18,7 @@
 
 using System;
 using System.ComponentModel;
+using System.Linq;
 
 using Avalonia;
 using Avalonia.Controls;
@@ -100,6 +101,17 @@ namespace ICSharpCode.ILSpy.TextView
 				FontFamily = new FontFamily(displaySettings.SelectedFont);
 			if (displaySettings.SelectedFontSize > 0)
 				FontSize = EditorZoom.EffectiveFontSize(displaySettings);
+			PrepareLineNumberMarginsForRender();
+		}
+
+		internal void PrepareLineNumberMarginsForRender()
+		{
+			foreach (var margin in TextArea.LeftMargins.OfType<LineNumberMargin>())
+			{
+				margin.SetValue(TextBlock.FontFamilyProperty, FontFamily);
+				margin.SetValue(TextBlock.FontSizeProperty, FontSize);
+				margin.Measure(new Size(double.PositiveInfinity, double.PositiveInfinity));
+			}
 		}
 
 		static DisplaySettings? TryGetDisplaySettings()
diff --git a/ILSpy/TextView/DecompilerTextView.axaml.cs b/ILSpy/TextView/DecompilerTextView.axaml.cs
index 4cc7feba1..3293f14da 100644
--- a/ILSpy/TextView/DecompilerTextView.axaml.cs
+++ b/ILSpy/TextView/DecompilerTextView.axaml.cs
@@ -34,6 +34,7 @@ using Avalonia.Threading;
 using Avalonia.VisualTree;
 
 using AvaloniaEdit.Document;
+using AvaloniaEdit.Editing;
 using AvaloniaEdit.Folding;
 using AvaloniaEdit.Highlighting;
 
@@ -179,6 +180,41 @@ namespace ICSharpCode.ILSpy.TextView
 				margin.Cursor = ArrowCursor;
 		}
 
+		void KeepBookmarkMarginBeforeLineNumbers()
+		{
+			if (bookmarkMargin == null)
+				return;
+
+			var margins = Editor.TextArea.LeftMargins;
+			var lineNumberIndex = -1;
+			for (var i = 0; i < margins.Count; i++)
+			{
+				if (margins[i] is LineNumberMargin)
+				{
+					lineNumberIndex = i;
+					break;
+				}
+			}
+			var bookmarkIndex = margins.IndexOf(bookmarkMargin);
+			if (lineNumberIndex < 0 || bookmarkIndex < 0 || bookmarkIndex < lineNumberIndex)
+				return;
+
+			var lineNumberMargin = margins[lineNumberIndex];
+			Control? separator = null;
+			if (lineNumberIndex + 1 < margins.Count
+				&& margins[lineNumberIndex + 1] is global::Avalonia.Controls.Shapes.Line)
+				separator = margins[lineNumberIndex + 1];
+
+			if (separator != null)
+				margins.Remove(separator);
+			margins.Remove(lineNumberMargin);
+
+			bookmarkIndex = margins.IndexOf(bookmarkMargin);
+			margins.Insert(bookmarkIndex + 1, lineNumberMargin);
+			if (separator != null)
+				margins.Insert(bookmarkIndex + 2, separator);
+		}
+
 		void OnPreviewKeyDownForOmnibar(object? sender, KeyEventArgs e)
 		{
 			if (e.Key == Key.L && e.KeyModifiers == KeyModifiers.Control && Omnibar.IsVisible)
@@ -649,6 +685,11 @@ namespace ICSharpCode.ILSpy.TextView
 			{
 				case nameof(DisplaySettings.ShowLineNumbers):
 					Editor.ShowLineNumbers = s.ShowLineNumbers;
+					if (Editor.ShowLineNumbers)
+					{
+						KeepBookmarkMarginBeforeLineNumbers();
+						Editor.PrepareLineNumberMarginsForRender();
+					}
 					break;
 				case nameof(DisplaySettings.EnableWordWrap):
 					Editor.WordWrap = s.EnableWordWrap;