diff --git a/bundles/org.eclipse.swt/Eclipse SWT/gtk/org/eclipse/swt/widgets/Display.java b/bundles/org.eclipse.swt/Eclipse SWT/gtk/org/eclipse/swt/widgets/Display.java
index 1b7539be33d..5d5f4019d38 100644
--- a/bundles/org.eclipse.swt/Eclipse SWT/gtk/org/eclipse/swt/widgets/Display.java	
+++ b/bundles/org.eclipse.swt/Eclipse SWT/gtk/org/eclipse/swt/widgets/Display.java	
@@ -199,6 +199,9 @@ public class Display extends Device implements Executor {
 	Shell activeShell;
 	boolean activePending;
 	boolean ignoreFocus;
+	/* GTK4: depth of focusProc() calls, and popovers disposed meanwhile, see Shell.releaseHandle() */
+	int focusProcDepth;
+	ArrayList<Long> disposedPopovers = new ArrayList<>();
 
 	Tracker tracker;
 
@@ -6149,7 +6152,32 @@ boolean scrollProc(long controller, double dx, double dy, long user_data) {
 	long handle = GTK.gtk_event_controller_get_widget(controller);
 	Widget widget = getWidget(handle);
 
-	if (widget != null) widget.focusProc(controller, user_data);
+	if (widget == null) return;
+	focusProcDepth++;
+	try {
+		widget.focusProc(controller, user_data);
+	} finally {
+		// GTK goes on with the focus change after this, so destroy the popovers later
+		if (--focusProcDepth == 0 && !disposedPopovers.isEmpty() && !isDisposed()) asyncExec(this::destroyDisposedPopovers);
+	}
+}
+
+/**
+ * GTK4: destroys the popovers of shells disposed while a focus change was dispatched.
+ */
+void destroyDisposedPopovers () {
+	// Still in a focus change, e.g. in a nested event loop of a listener, see focusProc()
+	if (focusProcDepth > 0) return;
+	ArrayList<Long> popovers = disposedPopovers;
+	disposedPopovers = new ArrayList<>();
+	for (long popover : popovers) {
+		// The parent window may have destroyed the popover meanwhile
+		if (GTK.gtk_widget_get_parent (popover) != 0) {
+			GTK.gtk_popover_popdown (popover);
+			GTK.gtk_widget_unparent (popover);
+		}
+		OS.g_object_unref (popover);
+	}
 }
 
 void windowActiveProc(long handle, long user_data) {;
diff --git a/bundles/org.eclipse.swt/Eclipse SWT/gtk/org/eclipse/swt/widgets/Shell.java b/bundles/org.eclipse.swt/Eclipse SWT/gtk/org/eclipse/swt/widgets/Shell.java
index f9053a3bb42..0089e907e31 100644
--- a/bundles/org.eclipse.swt/Eclipse SWT/gtk/org/eclipse/swt/widgets/Shell.java	
+++ b/bundles/org.eclipse.swt/Eclipse SWT/gtk/org/eclipse/swt/widgets/Shell.java	
@@ -3854,9 +3854,17 @@ void releaseHandle () {
 		 * its parent is released with destroy=false, which calls releaseHandle() but not
 		 * destroyWidget(); unparenting here covers both paths and avoids leaving the popover
 		 * attached to a finalizing parent window.
+		 *
+		 * GTK sends the focus leave events walking up the widget tree from the old focus
+		 * widget, so a popover disposed by a FocusOut listener is hidden and unparented
+		 * only once that focus change is done, see Display.focusProc().
 		 */
-		GTK.gtk_popover_popdown (shellHandle);
-		GTK.gtk_widget_unparent (shellHandle);
+		if (display.focusProcDepth > 0) {
+			display.disposedPopovers.add (OS.g_object_ref (shellHandle));
+		} else {
+			GTK.gtk_popover_popdown (shellHandle);
+			GTK.gtk_widget_unparent (shellHandle);
+		}
 	}
 	super.releaseHandle ();
 	shellHandle = 0;
diff --git a/tests/org.eclipse.swt.tests/JUnit Tests/org/eclipse/swt/tests/junit/Test_org_eclipse_swt_widgets_Shell.java b/tests/org.eclipse.swt.tests/JUnit Tests/org/eclipse/swt/tests/junit/Test_org_eclipse_swt_widgets_Shell.java
index cb403fdb2d5..623b52613b6 100644
--- a/tests/org.eclipse.swt.tests/JUnit Tests/org/eclipse/swt/tests/junit/Test_org_eclipse_swt_widgets_Shell.java	
+++ b/tests/org.eclipse.swt.tests/JUnit Tests/org/eclipse/swt/tests/junit/Test_org_eclipse_swt_widgets_Shell.java	
@@ -1,5 +1,5 @@
 /*******************************************************************************
- * Copyright (c) 2000, 2025 IBM Corporation and others.
+ * Copyright (c) 2000, 2026 IBM Corporation and others.
  *
  * This program and the accompanying materials
  * are made available under the terms of the Eclipse Public License 2.0
@@ -1063,6 +1063,28 @@ public void test_Issue450_NoShellActivateOnSetFocus() {
 	}
 }
 
+@Test
+public void test_onTopChildShellDisposedInFocusOut() throws InterruptedException {
+	shell.setLayout(new FillLayout());
+	Text text = new Text(shell, SWT.BORDER);
+	shell.open();
+	SwtTestUtil.processEvents();
+
+	Shell popup = new Shell(shell, SWT.ON_TOP | SWT.TOOL);
+	popup.setLayout(new FillLayout());
+	Text popupText = new Text(popup, SWT.BORDER);
+	popup.setSize(100, 100);
+	// Close when the focus leaves, as popups do
+	popupText.addListener(SWT.FocusOut, e -> popup.dispose());
+	popup.open();
+	popupText.forceFocus();
+	SwtTestUtil.processEvents();
+
+	text.forceFocus();
+	SwtTestUtil.processEvents(1000, popup::isDisposed);
+	assertTrue(popup.isDisposed());
+}
+
 @Test
 @Override
 public void test_setLocationLorg_eclipse_swt_graphics_Point() {