diff --git a/client/layout/sidebar/expandable.jsx b/client/layout/sidebar/expandable.jsx
index abefb6d1f10282..c1d6602cc6aadb 100644
--- a/client/layout/sidebar/expandable.jsx
+++ b/client/layout/sidebar/expandable.jsx
@@ -3,7 +3,7 @@
  */
 import classNames from 'classnames';
 import PropTypes from 'prop-types';
-import React from 'react';
+import React, { useState, useRef, useLayoutEffect } from 'react';
 import { get, uniqueId } from 'lodash';
 
 /**
@@ -12,6 +12,10 @@ import { get, uniqueId } from 'lodash';
 import TranslatableString from 'calypso/components/translatable/proptype';
 import ExpandableSidebarHeading from './expandable-heading';
 import SidebarMenu from 'calypso/layout/sidebar/menu';
+import { hasTouch } from 'calypso/lib/touch-detect';
+import config from 'calypso/config';
+
+const isTouch = hasTouch();
 
 function containsSelectedSidebarItem( children ) {
 	let selectedItemFound = false;
@@ -35,6 +39,11 @@ function containsSelectedSidebarItem( children ) {
 	return selectedItemFound;
 }
 
+const offScreen = ( submenu ) => {
+	const rect = submenu.getBoundingClientRect();
+	return rect.y + rect.height > window.innerHeight;
+};
+
 export const ExpandableSidebarMenu = ( {
 	className,
 	title,
@@ -48,6 +57,14 @@ export const ExpandableSidebarMenu = ( {
 	...props
 } ) => {
 	let { expanded } = props;
+	const submenu = useRef();
+	const [ submenuHovered, setSubmenuHovered ] = useState( false );
+
+	if ( submenu.current ) {
+		// Sets flyout to expand towards bottom
+		submenu.current.style.bottom = 'auto';
+		submenu.current.style.top = 0;
+	}
 
 	if ( null === expanded ) {
 		expanded = containsSelectedSidebarItem( children );
@@ -56,12 +73,41 @@ export const ExpandableSidebarMenu = ( {
 	const classes = classNames( className, {
 		'is-toggle-open': !! expanded,
 		'is-togglable': true,
+		hovered: submenuHovered,
 	} );
 
+	const onEnter = () => {
+		if ( expanded || isTouch ) {
+			return;
+		}
+
+		setSubmenuHovered( true );
+	};
+
+	const onLeave = () => {
+		if ( expanded || isTouch ) {
+			return;
+		}
+
+		setSubmenuHovered( false );
+	};
+
 	const menuId = uniqueId( 'menu' );
 
+	useLayoutEffect( () => {
+		if ( submenuHovered && offScreen( submenu.current ) ) {
+			// Sets flyout to expand towards top
+			submenu.current.style.bottom = 0;
+			submenu.current.style.top = 'auto';
+		}
+	}, [ submenuHovered ] );
+
 	return (
-		<SidebarMenu className={ classes }>
+		<SidebarMenu
+			className={ classes }
+			onMouseEnter={ config.isEnabled( 'nav-unification' ) ? () => onEnter() : null }
+			onMouseLeave={ config.isEnabled( 'nav-unification' ) ? () => onLeave() : null }
+		>
 			<ExpandableSidebarHeading
 				title={ title }
 				count={ count }
@@ -74,7 +120,13 @@ export const ExpandableSidebarMenu = ( {
 				menuId={ menuId }
 				{ ...props }
 			/>
-			<li role="region" id={ menuId } className="sidebar__expandable-content" hidden={ ! expanded }>
+			<li
+				role="region"
+				ref={ submenu }
+				id={ menuId }
+				className="sidebar__expandable-content"
+				hidden={ ! expanded }
+			>
 				<ul>{ children }</ul>
 			</li>
 		</SidebarMenu>
diff --git a/client/layout/sidebar/menu.jsx b/client/layout/sidebar/menu.jsx
index 3a76ecc6807cba..be69d6fee12f2f 100644
--- a/client/layout/sidebar/menu.jsx
+++ b/client/layout/sidebar/menu.jsx
@@ -5,8 +5,10 @@
 import React from 'react';
 import classNames from 'classnames';
 
-const SidebarMenu = ( { children, className } ) => (
-	<ul className={ classNames( 'sidebar__menu', className ) }>{ children }</ul>
+const SidebarMenu = ( { children, className, ...props } ) => (
+	<ul className={ classNames( 'sidebar__menu', className ) } { ...props }>
+		{ children }
+	</ul>
 );
 
 export default SidebarMenu;
diff --git a/client/my-sites/sidebar-unified/menu.jsx b/client/my-sites/sidebar-unified/menu.jsx
index 3e5f7bfc457dd1..171ab348e16b3d 100644
--- a/client/my-sites/sidebar-unified/menu.jsx
+++ b/client/my-sites/sidebar-unified/menu.jsx
@@ -60,38 +60,40 @@ export const MySitesSidebarUnifiedMenu = ( {
 	}, [ selected, childIsSelected, reduxDispatch, sectionId, sidebarCollapsed ] );
 
 	return (
-		<ExpandableSidebarMenu
-			onClick={ () => {
-				if ( link ) {
-					if ( isExternal( link ) ) {
-						// If the URL is external, page() will fail to replace state between different domains
-						externalRedirect( link );
-						return;
+		<li>
+			<ExpandableSidebarMenu
+				onClick={ () => {
+					if ( link ) {
+						if ( isExternal( link ) ) {
+							// If the URL is external, page() will fail to replace state between different domains.
+							externalRedirect( link );
+							return;
+						}
+						page( link );
 					}
-					page( link );
-				}
-				if ( ! sidebarCollapsed ) {
-					reduxDispatch( collapseAllMySitesSidebarSections() );
-					reduxDispatch( toggleSection( sectionId ) );
-				}
-			} }
-			expanded={ ! sidebarCollapsed && isExpanded }
-			title={ title }
-			customIcon={ <SidebarCustomIcon icon={ icon } /> }
-			className={ ( selected || childIsSelected ) && 'sidebar__menu--selected' }
-		>
-			{ children.map( ( item ) => {
-				const isSelected = selectedMenuItem?.url === item.url;
-				return (
-					<MySitesSidebarUnifiedItem
-						key={ item.slug }
-						{ ...item }
-						selected={ isSelected }
-						isSubItem={ true }
-					/>
-				);
-			} ) }
-		</ExpandableSidebarMenu>
+					if ( ! sidebarCollapsed ) {
+						reduxDispatch( collapseAllMySitesSidebarSections() );
+						reduxDispatch( toggleSection( sectionId ) );
+					}
+				} }
+				expanded={ ! sidebarCollapsed && isExpanded }
+				title={ title }
+				customIcon={ <SidebarCustomIcon icon={ icon } /> }
+				className={ ( selected || childIsSelected ) && 'sidebar__menu--selected' }
+			>
+				{ children.map( ( item ) => {
+					const isSelected = selectedMenuItem?.url === item.url;
+					return (
+						<MySitesSidebarUnifiedItem
+							key={ item.slug }
+							{ ...item }
+							selected={ isSelected }
+							isSubItem={ true }
+						/>
+					);
+				} ) }
+			</ExpandableSidebarMenu>
+		</li>
 	);
 };
 
diff --git a/client/my-sites/sidebar-unified/style.scss b/client/my-sites/sidebar-unified/style.scss
index e4945d3a94df0a..49f35dadd578ab 100644
--- a/client/my-sites/sidebar-unified/style.scss
+++ b/client/my-sites/sidebar-unified/style.scss
@@ -483,7 +483,8 @@ $font-size: rem( 14px );
 			}
 		}
 
-		.sidebar__menu.is-togglable:not( .is-toggle-open ):hover {
+		.sidebar__menu.is-togglable:not( .is-toggle-open ).hovered {
+			// .hovered is handled in client/layout/sidebar/expandable.jsx. Needed for repositioning and hover intent.
 			position: relative;
 
 			.sidebar__heading {
@@ -500,8 +501,9 @@ $font-size: rem( 14px );
 			// flyout content
 			.sidebar__expandable-content {
 				display: block;
-				position: absolute;
 				top: 0;
+				bottom: auto;
+				position: absolute;
 				left: var( --sidebar-width-max );
 				width: 160px;
 
diff --git a/client/my-sites/sidebar/test/sidebar.js b/client/my-sites/sidebar/test/sidebar.js
index 00782a4330839d..74880e918b464e 100644
--- a/client/my-sites/sidebar/test/sidebar.js
+++ b/client/my-sites/sidebar/test/sidebar.js
@@ -1,3 +1,7 @@
+/**
+ * @jest-environment jsdom
+ */
+
 /**
  * External dependencies
  */