diff --git a/src/Controls/src/Core/Compatibility/Handlers/NavigationPage/iOS/NavigationRenderer.cs b/src/Controls/src/Core/Compatibility/Handlers/NavigationPage/iOS/NavigationRenderer.cs
index 54366c0e1c15..c6e0c46e39e8 100644
--- a/src/Controls/src/Core/Compatibility/Handlers/NavigationPage/iOS/NavigationRenderer.cs
+++ b/src/Controls/src/Core/Compatibility/Handlers/NavigationPage/iOS/NavigationRenderer.cs
@@ -627,7 +627,14 @@ void InsertPageBefore(Page page, Page before)
 
 			var pageContainer = CreateViewControllerForPage(page);
 			var target = nvh.ViewController.ParentViewController;
-			ViewControllers = ViewControllers.Insert(ViewControllers.IndexOf(target), pageContainer);
+			var index = ViewControllers.IndexOf(target);
+			ViewControllers = ViewControllers.Insert(index, pageContainer);
+
+			// Update the flyout icon when the root page changes
+			if (index == 0)
+			{
+				(target as ParentingViewController)?.UpdateLeftBarButtonItem();
+			}
 		}
 
 		void OnInsertPageBeforeRequested(object sender, NavigationRequestedEventArgs e)
@@ -1506,8 +1513,7 @@ internal void UpdateLeftBarButtonItem(Page pageBeingRemoved = null)
 					return;
 
 				var currentChild = this.Child;
-				var firstPage = n.NavPageController.Pages.FirstOrDefault();
-
+				var firstPage = (n.ViewControllers.FirstOrDefault() as ParentingViewController)?.Child;
 
 				if (n._parentFlyoutPage == null)
 					return;
diff --git a/src/Controls/tests/TestCases.Android.Tests/snapshots/android/FlyoutIconUpdatedAfterInsertPageBefore.png b/src/Controls/tests/TestCases.Android.Tests/snapshots/android/FlyoutIconUpdatedAfterInsertPageBefore.png
new file mode 100644
index 000000000000..fc801b91b578
Binary files /dev/null and b/src/Controls/tests/TestCases.Android.Tests/snapshots/android/FlyoutIconUpdatedAfterInsertPageBefore.png differ
diff --git a/src/Controls/tests/TestCases.HostApp/Issues/Issue29921.cs b/src/Controls/tests/TestCases.HostApp/Issues/Issue29921.cs
new file mode 100644
index 000000000000..95c10469bde4
--- /dev/null
+++ b/src/Controls/tests/TestCases.HostApp/Issues/Issue29921.cs
@@ -0,0 +1,63 @@
+namespace Maui.Controls.Sample.Issues;
+
+[Issue(IssueTracker.Github, 29921, "Flyout icon not replaced after root page change", PlatformAffected.iOS)]
+public class Issue29921 : FlyoutPage
+{
+	public Issue29921()
+	{
+		Detail = new NavigationPage(new Issue29921Page1());
+		Flyout = new ContentPage
+		{
+			Title = "Flyout Page",
+			IconImageSource = "menu_icon.png",
+			Content = new Label
+			{
+				Text = "This is flyout",
+				VerticalOptions = LayoutOptions.Center,
+				HorizontalOptions = LayoutOptions.Center
+			}
+		};
+		FlyoutLayoutBehavior = FlyoutLayoutBehavior.Popover;
+	}
+}
+
+public class Issue29921Page1 : ContentPage
+{
+	public Issue29921Page1()
+	{
+		Title = "Page 1";
+		var insertBeforeButton = new Button { Text = "Insert Page Before", AutomationId = "InsertPageButton" };
+		insertBeforeButton.Clicked += InsertBefore_Clicked;
+		Content = new StackLayout
+		{
+			VerticalOptions = LayoutOptions.Center,
+			HorizontalOptions = LayoutOptions.Center,
+			Children = { insertBeforeButton }
+		};
+	}
+
+	private void InsertBefore_Clicked(object sender, EventArgs e)
+	{
+		if (Parent is NavigationPage navPage)
+		{
+			navPage.Navigation.InsertPageBefore(new Issue29921Page2(), navPage.RootPage);
+		}
+	}
+}
+
+public class Issue29921Page2 : ContentPage
+{
+	public Issue29921Page2()
+	{
+		Title = "Page 2";
+		Content = new StackLayout
+		{
+			VerticalOptions = LayoutOptions.Center,
+			HorizontalOptions = LayoutOptions.Center,
+			Children =
+				{
+					new Label { Text = "Flyout icon is visible", AutomationId = "Page2Label" },
+				}
+		};
+	}
+}
diff --git a/src/Controls/tests/TestCases.Mac.Tests/snapshots/mac/FlyoutIconUpdatedAfterInsertPageBefore.png b/src/Controls/tests/TestCases.Mac.Tests/snapshots/mac/FlyoutIconUpdatedAfterInsertPageBefore.png
new file mode 100644
index 000000000000..f78fcba49019
Binary files /dev/null and b/src/Controls/tests/TestCases.Mac.Tests/snapshots/mac/FlyoutIconUpdatedAfterInsertPageBefore.png differ
diff --git a/src/Controls/tests/TestCases.Shared.Tests/Tests/Issues/Issue29921.cs b/src/Controls/tests/TestCases.Shared.Tests/Tests/Issues/Issue29921.cs
new file mode 100644
index 000000000000..d0bebe9a58a2
--- /dev/null
+++ b/src/Controls/tests/TestCases.Shared.Tests/Tests/Issues/Issue29921.cs
@@ -0,0 +1,22 @@
+using NUnit.Framework;
+using UITest.Appium;
+using UITest.Core;
+
+namespace Microsoft.Maui.TestCases.Tests.Issues;
+
+public class Issue29921 : _IssuesUITest
+{
+	public Issue29921(TestDevice testDevice) : base(testDevice)
+	{
+	}
+	public override string Issue => "Flyout icon not replaced after root page change";
+
+	[Test]
+	[Category(UITestCategories.FlyoutPage)]
+	public void FlyoutIconUpdatedAfterInsertPageBefore()
+	{
+		App.WaitForElement("InsertPageButton");
+		App.Tap("InsertPageButton");
+		VerifyScreenshot();
+	}
+}
\ No newline at end of file
diff --git a/src/Controls/tests/TestCases.WinUI.Tests/snapshots/windows/FlyoutIconUpdatedAfterInsertPageBefore.png b/src/Controls/tests/TestCases.WinUI.Tests/snapshots/windows/FlyoutIconUpdatedAfterInsertPageBefore.png
new file mode 100644
index 000000000000..6209512d91b0
Binary files /dev/null and b/src/Controls/tests/TestCases.WinUI.Tests/snapshots/windows/FlyoutIconUpdatedAfterInsertPageBefore.png differ
diff --git a/src/Controls/tests/TestCases.iOS.Tests/snapshots/ios/FlyoutIconUpdatedAfterInsertPageBefore.png b/src/Controls/tests/TestCases.iOS.Tests/snapshots/ios/FlyoutIconUpdatedAfterInsertPageBefore.png
new file mode 100644
index 000000000000..112a4f1c0e1a
Binary files /dev/null and b/src/Controls/tests/TestCases.iOS.Tests/snapshots/ios/FlyoutIconUpdatedAfterInsertPageBefore.png differ