diff --git a/packages/edit-post/src/components/visual-editor/index.js b/packages/edit-post/src/components/visual-editor/index.js
index fe14ef0556113..f888630afeca1 100644
--- a/packages/edit-post/src/components/visual-editor/index.js
+++ b/packages/edit-post/src/components/visual-editor/index.js
@@ -334,11 +334,19 @@ export default function VisualEditor( { styles } ) {
 		.is-root-container.alignfull { max-width: none; margin-left: auto; margin-right: auto;}
 		.is-root-container.alignfull:where(.is-layout-flow) > :not(.alignleft):not(.alignright) { max-width: none;}`;
 
+	const isToBeIframed =
+		( ( hasV3BlocksOnly || ( isGutenbergPlugin && isBlockBasedTheme ) ) &&
+			! hasMetaBoxes ) ||
+		isTemplateMode ||
+		deviceType === 'Tablet' ||
+		deviceType === 'Mobile';
+
 	return (
 		<BlockTools
 			__unstableContentRef={ ref }
 			className={ classnames( 'edit-post-visual-editor', {
 				'is-template-mode': isTemplateMode,
+				'has-inline-canvas': ! isToBeIframed,
 			} ) }
 		>
 			<motion.div
@@ -354,14 +362,7 @@ export default function VisualEditor( { styles } ) {
 					className={ previewMode }
 				>
 					<MaybeIframe
-						shouldIframe={
-							( ( hasV3BlocksOnly ||
-								( isGutenbergPlugin && isBlockBasedTheme ) ) &&
-								! hasMetaBoxes ) ||
-							isTemplateMode ||
-							deviceType === 'Tablet' ||
-							deviceType === 'Mobile'
-						}
+						shouldIframe={ isToBeIframed }
 						contentRef={ contentRef }
 						styles={ styles }
 					>
diff --git a/packages/edit-post/src/components/visual-editor/style.scss b/packages/edit-post/src/components/visual-editor/style.scss
index 00678f9867ec3..fa61cc9889cf9 100644
--- a/packages/edit-post/src/components/visual-editor/style.scss
+++ b/packages/edit-post/src/components/visual-editor/style.scss
@@ -2,7 +2,11 @@
 	position: relative;
 	display: flex;
 	flex-flow: column;
-	overflow: hidden;
+	// In the iframed canvas this keeps extra scrollbars from appearing (when block toolbars overflow). In the
+	// legacy (non-iframed) canvas, overflow must not be hidden in order to maintain support for sticky positioning.
+	&:not(.has-inline-canvas) {
+		overflow: hidden;
+	}
 
 	// Gray preview overlay (desktop/tablet/mobile) is intentionally not set on an element with scrolling content like
 	// interface-interface-skeleton__content. This causes graphical glitches (flashes of the background color)