diff --git a/packages/customize-widgets/src/components/sidebar-block-editor/style.scss b/packages/customize-widgets/src/components/sidebar-block-editor/style.scss
index abbe6b84454103..3f9ea52021d984 100644
--- a/packages/customize-widgets/src/components/sidebar-block-editor/style.scss
+++ b/packages/customize-widgets/src/components/sidebar-block-editor/style.scss
@@ -13,6 +13,14 @@
 }
 
 .customize-control-sidebar_block_editor .block-editor-block-list__block-popover {
-	position: fixed;
+	// FloatingUI library used in Popover component forces us to have an "absolute" inline style.
+	// We need to override this in the customizer.
+	position: fixed !important;
 	z-index: z-index(".customize-widgets__block-toolbar");
 }
+
+.customize-widgets-popover .components-popover {
+	// FloatingUI library used in Popover component forces us to have an "absolute" inline style.
+	// We need to override this in the customizer.
+	position: fixed !important;
+}
diff --git a/test/e2e/specs/widgets/customizing-widgets.spec.js b/test/e2e/specs/widgets/customizing-widgets.spec.js
index d584e05465dafb..f7907da35494bc 100644
--- a/test/e2e/specs/widgets/customizing-widgets.spec.js
+++ b/test/e2e/specs/widgets/customizing-widgets.spec.js
@@ -52,6 +52,11 @@ test.describe( 'Widgets Customizer', () => {
 			)
 		).toBeVisible();
 
+		// Clear block selection, so the block toolbar isn't visible.
+		await page.evaluate( () => {
+			window.wp.data.dispatch( 'core/block-editor' ).clearSelectedBlock();
+		} );
+
 		await widgetsCustomizerPage.addBlock( 'Heading' );
 		await page.keyboard.type( 'My Heading' );