diff --git a/src/Uno.UI.RuntimeTests/Tests/Windows_UI_Xaml_Controls/Given_TextBox.cs b/src/Uno.UI.RuntimeTests/Tests/Windows_UI_Xaml_Controls/Given_TextBox.cs
index a25f8b786c71..a34dd21378a8 100644
--- a/src/Uno.UI.RuntimeTests/Tests/Windows_UI_Xaml_Controls/Given_TextBox.cs
+++ b/src/Uno.UI.RuntimeTests/Tests/Windows_UI_Xaml_Controls/Given_TextBox.cs
@@ -28,6 +28,7 @@
 using Windows.UI.Input.Preview.Injection;
 using Windows.Foundation;
 using System.Collections.Generic;
+using Uno.Extensions;
 
 
 #if WINAPPSDK
@@ -1124,6 +1125,44 @@ static FrameworkElement GetSCP(TextBox tb)
 		}
 #endif
 
+#if HAS_UNO
+		[TestMethod]
+		[UnoWorkItem("https://github.com/unoplatform/uno/issues/18790")]
+#if !HAS_INPUT_INJECTOR
+		[Ignore("InputInjector is not supported on this platform.")]
+#endif
+		public async Task When_Clicked_In_Popup()
+		{
+			TextBox tb;
+			var btn = new Button
+			{
+				Flyout = new Flyout
+				{
+					Content = tb = new TextBox()
+				}
+			};
+
+			await UITestHelper.Load(btn);
+
+			var injector = InputInjector.TryCreate() ?? throw new InvalidOperationException("Failed to init the InputInjector");
+			using var mouse = injector.GetMouse();
+
+			mouse.Press(btn.GetAbsoluteBoundsRect().GetCenter());
+			await UITestHelper.WaitForIdle();
+			mouse.Release();
+			await UITestHelper.WaitForIdle();
+
+			Assert.IsTrue(btn.Flyout.IsOpen);
+
+			mouse.Press(tb.GetAbsoluteBoundsRect().GetCenter());
+			await UITestHelper.WaitForIdle();
+			mouse.Release();
+			await UITestHelper.WaitForIdle();
+
+			Assert.AreEqual(tb, FocusManager.GetFocusedElement(WindowHelper.XamlRoot));
+		}
+#endif
+
 		private static async Task<TextBox> LoadZeroSizeTextBoxAsync(Style style)
 		{
 			var loaded = false;
diff --git a/src/Uno.UI/UI/Xaml/Controls/ScrollViewer/ScrollViewer.MuxInternal.cs b/src/Uno.UI/UI/Xaml/Controls/ScrollViewer/ScrollViewer.MuxInternal.cs
index da055cd0aa8a..f46d339ba603 100644
--- a/src/Uno.UI/UI/Xaml/Controls/ScrollViewer/ScrollViewer.MuxInternal.cs
+++ b/src/Uno.UI/UI/Xaml/Controls/ScrollViewer/ScrollViewer.MuxInternal.cs
@@ -179,6 +179,13 @@ protected override void OnPointerReleased(PointerRoutedEventArgs args)
 
 		private static bool ScrollContentControl_SetFocusOnFlyoutLightDismissPopupByPointer(UIElement pScrollContentControl)
 		{
+#if __WASM__
+			if ((pScrollContentControl as ScrollViewer)?.DisableSetFocusOnPopupByPointer ?? false)
+			{
+				return false;
+			}
+#endif
+
 			PopupRoot? pPopupRoot = null;
 			Popup? pPopup = null;
 
diff --git a/src/Uno.UI/UI/Xaml/Controls/ScrollViewer/ScrollViewer.wasm.cs b/src/Uno.UI/UI/Xaml/Controls/ScrollViewer/ScrollViewer.wasm.cs
index e709cb5ac605..185369d583cd 100644
--- a/src/Uno.UI/UI/Xaml/Controls/ScrollViewer/ScrollViewer.wasm.cs
+++ b/src/Uno.UI/UI/Xaml/Controls/ScrollViewer/ScrollViewer.wasm.cs
@@ -11,6 +11,15 @@ namespace Microsoft.UI.Xaml.Controls
 {
 	partial class ScrollViewer
 	{
+		/// <summary>
+		/// This is specifically added for ScrollViewers inside TextBoxes and specifically for WASM
+		/// On WASM, a click on a TextBox inside a popup shifts focus to the Popup instead of the TextBox
+		/// as a result of ScrollContentControl_SetFocusOnFlyoutLightDismissPopupByPointer.
+		/// This is only a problem on WASM because we don't capture the pointer when pressing inside a TextBox
+		/// <seealso cref="TextBox.IsPointerCaptureRequired"/>.
+		/// </summary>
+		internal bool DisableSetFocusOnPopupByPointer { get; set; }
+
 		internal bool CancelNextNativeScroll { get; private set; }
 		internal Size ScrollBarSize => (_presenter as ScrollContentPresenter)?.ScrollBarSize ?? default;
 
diff --git a/src/Uno.UI/UI/Xaml/Controls/TextBox/TextBox.Uno.cs b/src/Uno.UI/UI/Xaml/Controls/TextBox/TextBox.Uno.cs
index f2d61ea1b0f1..d4ae5cc37679 100644
--- a/src/Uno.UI/UI/Xaml/Controls/TextBox/TextBox.Uno.cs
+++ b/src/Uno.UI/UI/Xaml/Controls/TextBox/TextBox.Uno.cs
@@ -28,6 +28,16 @@ public bool IsPointerCaptureRequired
 			new FrameworkPropertyMetadata(
 				// We should not capture the pointer on WASM by default because it would prevent the user from scrolling through text on selection.
 				// See https://github.com/unoplatform/uno/pull/16982, https://issues.chromium.org/issues/344491566
-				false));
+				false
+#if __WASM__
+				, static (dO, args) =>
+				{
+					if (((TextBox)dO)._contentElement is ScrollViewer sv)
+					{
+						sv.DisableSetFocusOnPopupByPointer = !(bool)args.NewValue;
+					}
+				}
+#endif
+			));
 #endif
 }
diff --git a/src/Uno.UI/UI/Xaml/Controls/TextBox/TextBox.cs b/src/Uno.UI/UI/Xaml/Controls/TextBox/TextBox.cs
index 18bc396a19d0..8af394c29f34 100644
--- a/src/Uno.UI/UI/Xaml/Controls/TextBox/TextBox.cs
+++ b/src/Uno.UI/UI/Xaml/Controls/TextBox/TextBox.cs
@@ -171,6 +171,10 @@ private protected override void OnLoaded()
 					scrollViewer.HorizontalScrollBarVisibility = ScrollBarVisibility.Disabled; // The template sets this to Hidden
 					scrollViewer.VerticalScrollBarVisibility = ScrollBarVisibility.Auto; // The template sets this to Hidden
 				}
+
+#if __WASM__
+				scrollViewer.DisableSetFocusOnPopupByPointer = !IsPointerCaptureRequired;
+#endif
 #endif
 			}
 		}