diff --git a/packages/block-library/src/legacy-widget/edit/preview.js b/packages/block-library/src/legacy-widget/edit/preview.js
index 5f884aa117fb34..639d7a6d0874e2 100644
--- a/packages/block-library/src/legacy-widget/edit/preview.js
+++ b/packages/block-library/src/legacy-widget/edit/preview.js
@@ -6,13 +6,44 @@ import classnames from 'classnames';
 /**
  * WordPress dependencies
  */
+import { useRefEffect } from '@wordpress/compose';
 import { addQueryArgs } from '@wordpress/url';
 import { useState } from '@wordpress/element';
 import { Placeholder, Spinner, Disabled } from '@wordpress/components';
 import { __ } from '@wordpress/i18n';
 
 export default function Preview( { idBase, instance, isVisible } ) {
-	const [ iframeHeight, setIframeHeight ] = useState( null );
+	const [ iframeHeight, setIframeHeight ] = useState();
+
+	// Resize the iframe on either the load event, or when the iframe becomes visible.
+	const ref = useRefEffect( ( iframe ) => {
+		function onChange() {
+			const boundingRect = iframe?.contentDocument?.body?.getBoundingClientRect();
+			if ( boundingRect ) {
+				// Include `top` in the height calculation to avoid the bottom
+				// of widget previews being cut-off. Most widgets have a
+				// heading at the top that has top margin, and the `height`
+				// alone doesn't take that margin into account.
+				setIframeHeight( boundingRect.top + boundingRect.height );
+			}
+		}
+
+		const { IntersectionObserver } = iframe.ownerDocument.defaultView;
+
+		// Observe for intersections that might cause a change in the height of
+		// the iframe, e.g. a Widget Area becoming expanded.
+		const intersectionObserver = new IntersectionObserver( onChange, {
+			threshold: 1,
+		} );
+		intersectionObserver.observe( iframe );
+
+		iframe.addEventListener( 'load', onChange );
+
+		return () => {
+			iframe.removeEventListener( 'load', onChange );
+		};
+	}, [] );
+
 	return (
 		<>
 			{ /*
@@ -41,6 +72,7 @@ export default function Preview( { idBase, instance, isVisible } ) {
 					load scripts and styles that it needs to run.
 					*/ }
 					<iframe
+						ref={ ref }
 						className="wp-block-legacy-widget__edit-preview-iframe"
 						title={ __( 'Legacy Widget Preview' ) }
 						// TODO: This chokes when the query param is too big.
@@ -53,12 +85,7 @@ export default function Preview( { idBase, instance, isVisible } ) {
 								instance,
 							},
 						} ) }
-						height={ iframeHeight ?? 100 }
-						onLoad={ ( event ) => {
-							setIframeHeight(
-								event.target.contentDocument.body.scrollHeight
-							);
-						} }
+						height={ iframeHeight || 100 }
 					/>
 				</Disabled>
 			</div>