diff --git a/public/app/core/components/AppChrome/AppChrome.tsx b/public/app/core/components/AppChrome/AppChrome.tsx
index a23b75fa50e..5f7bc35fe96 100644
--- a/public/app/core/components/AppChrome/AppChrome.tsx
+++ b/public/app/core/components/AppChrome/AppChrome.tsx
@@ -93,7 +93,7 @@ export function AppChrome({ children }: Props) {
       </main>
       {!state.chromeless && (
         <>
-          {config.featureToggles.dockedMegaMenu ? (
+          {config.featureToggles.dockedMegaMenu && state.megaMenu !== 'docked' ? (
             <AppChromeMenu />
           ) : (
             <MegaMenu searchBarHidden={searchBarHidden} onClose={() => chrome.setMegaMenu('closed')} />
diff --git a/public/app/core/components/AppChrome/AppChromeMenu.tsx b/public/app/core/components/AppChrome/AppChromeMenu.tsx
index a204e7fc9b3..d5718520bce 100644
--- a/public/app/core/components/AppChrome/AppChromeMenu.tsx
+++ b/public/app/core/components/AppChrome/AppChromeMenu.tsx
@@ -2,7 +2,7 @@ import { css } from '@emotion/css';
 import { useDialog } from '@react-aria/dialog';
 import { FocusScope } from '@react-aria/focus';
 import { OverlayContainer, useOverlay } from '@react-aria/overlays';
-import React, { useRef } from 'react';
+import React, { useEffect, useRef } from 'react';
 import CSSTransition from 'react-transition-group/CSSTransition';
 
 import { GrafanaTheme2 } from '@grafana/data';
@@ -20,11 +20,18 @@ export function AppChromeMenu({}: Props) {
   const theme = useTheme2();
   const { chrome } = useGrafana();
   const state = chrome.useState();
+  const prevMegaMenuState = useRef(state.megaMenu);
   const searchBarHidden = state.searchBarHidden || state.kioskMode === KioskMode.TV;
 
+  useEffect(() => {
+    prevMegaMenuState.current = state.megaMenu;
+  }, [state.megaMenu]);
+
   const ref = useRef(null);
   const backdropRef = useRef(null);
-  const animationSpeed = theme.transitions.duration.shortest;
+  // we don't want to show the opening animation when transitioning between docked + open
+  const animationSpeed =
+    prevMegaMenuState.current === 'docked' && state.megaMenu === 'open' ? 0 : theme.transitions.duration.shortest;
   const animationStyles = useStyles2(getAnimStyles, animationSpeed);
 
   const isOpen = state.megaMenu === 'open';
@@ -57,7 +64,7 @@ export function AppChromeMenu({}: Props) {
           classNames={animationStyles.overlay}
           timeout={{ enter: animationSpeed, exit: 0 }}
         >
-          <FocusScope contain autoFocus>
+          <FocusScope contain autoFocus restoreFocus>
             <MegaMenu className={styles.menu} onClose={onClose} ref={ref} {...overlayProps} {...dialogProps} />
           </FocusScope>
         </CSSTransition>
diff --git a/public/app/core/components/AppChrome/DockedMegaMenu/MegaMenu.tsx b/public/app/core/components/AppChrome/DockedMegaMenu/MegaMenu.tsx
index 1a15b5c01c5..61fc62ca533 100644
--- a/public/app/core/components/AppChrome/DockedMegaMenu/MegaMenu.tsx
+++ b/public/app/core/components/AppChrome/DockedMegaMenu/MegaMenu.tsx
@@ -35,7 +35,12 @@ export const MegaMenu = React.memo(
     const activeItem = getActiveItem(navItems, location.pathname);
 
     const handleDockedMenu = () => {
-      chrome.setMegaMenu(state.megaMenu === 'docked' ? 'closed' : 'docked');
+      chrome.setMegaMenu(state.megaMenu === 'docked' ? 'open' : 'docked');
+
+      // refocus on dock/undock button when changing state
+      setTimeout(() => {
+        document.getElementById('dock-menu-button')?.focus();
+      });
     };
 
     return (
@@ -54,21 +59,26 @@ export const MegaMenu = React.memo(
           <CustomScrollbar showScrollIndicators hideHorizontalTrack>
             <ul className={styles.itemList}>
               {navItems.map((link, index) => (
-                <Stack key={link.text} direction="row" alignItems="center">
-                  <MegaMenuItem
-                    link={link}
-                    onClick={state.megaMenu === 'open' ? onClose : undefined}
-                    activeItem={activeItem}
-                  />
-                  {index === 0 && Boolean(state.megaMenu === 'open') && (
+                <Stack key={link.text} direction={index === 0 ? 'row-reverse' : 'row'} alignItems="center">
+                  {index === 0 && (
                     <IconButton
+                      id="dock-menu-button"
                       className={styles.dockMenuButton}
-                      tooltip={t('navigation.megamenu.dock', 'Dock menu')}
+                      tooltip={
+                        state.megaMenu === 'docked'
+                          ? t('navigation.megamenu.undock', 'Undock menu')
+                          : t('navigation.megamenu.dock', 'Dock menu')
+                      }
                       name="web-section-alt"
                       onClick={handleDockedMenu}
                       variant="secondary"
                     />
                   )}
+                  <MegaMenuItem
+                    link={link}
+                    onClick={state.megaMenu === 'open' ? onClose : undefined}
+                    activeItem={activeItem}
+                  />
                 </Stack>
               ))}
             </ul>
diff --git a/public/app/core/components/AppChrome/NavToolbar/NavToolbar.tsx b/public/app/core/components/AppChrome/NavToolbar/NavToolbar.tsx
index 059d961b9a6..5d388544308 100644
--- a/public/app/core/components/AppChrome/NavToolbar/NavToolbar.tsx
+++ b/public/app/core/components/AppChrome/NavToolbar/NavToolbar.tsx
@@ -1,10 +1,11 @@
 import { css } from '@emotion/css';
-import React from 'react';
+import React, { useState } from 'react';
 
 import { GrafanaTheme2, NavModelItem } from '@grafana/data';
 import { Components } from '@grafana/e2e-selectors';
-import { Icon, IconButton, ToolbarButton, useStyles2 } from '@grafana/ui';
+import { Icon, IconButton, ToolbarButton, useStyles2, useTheme2 } from '@grafana/ui';
 import { useGrafana } from 'app/core/context/GrafanaContext';
+import { useMediaQueryChange } from 'app/core/hooks/useMediaQueryChange';
 import { t } from 'app/core/internationalization';
 import { HOME_NAV_ID } from 'app/core/reducers/navModel';
 import { useSelector } from 'app/types';
@@ -39,9 +40,22 @@ export function NavToolbar({
   const { chrome } = useGrafana();
   const state = chrome.useState();
   const homeNav = useSelector((state) => state.navIndex)[HOME_NAV_ID];
+  const theme = useTheme2();
   const styles = useStyles2(getStyles);
   const breadcrumbs = buildBreadcrumbs(sectionNav, pageNav, homeNav);
 
+  const dockMenuBreakpoint = theme.breakpoints.values.xl;
+  const [isTooSmallForDockedMenu, setIsTooSmallForDockedMenu] = useState(
+    !window.matchMedia(`(min-width: ${dockMenuBreakpoint}px)`).matches
+  );
+
+  useMediaQueryChange({
+    breakpoint: dockMenuBreakpoint,
+    onChange: (e) => {
+      setIsTooSmallForDockedMenu(!e.matches);
+    },
+  });
+
   return (
     <div data-testid={Components.NavToolbar.container} className={styles.pageToolbar}>
       <div className={styles.menuButton}>
@@ -49,7 +63,7 @@ export function NavToolbar({
           id={TOGGLE_BUTTON_ID}
           name="bars"
           tooltip={
-            state.megaMenu === 'closed'
+            state.megaMenu === 'closed' || (state.megaMenu === 'docked' && isTooSmallForDockedMenu)
               ? t('navigation.toolbar.open-menu', 'Open menu')
               : t('navigation.toolbar.close-menu', 'Close menu')
           }
diff --git a/public/locales/de-DE/grafana.json b/public/locales/de-DE/grafana.json
index 4b9e4b2fa0d..dcee13939eb 100644
--- a/public/locales/de-DE/grafana.json
+++ b/public/locales/de-DE/grafana.json
@@ -935,7 +935,8 @@
     },
     "megamenu": {
       "close": "Menü schließen",
-      "dock": "Menü andocken"
+      "dock": "Menü andocken",
+      "undock": ""
     },
     "toolbar": {
       "close-menu": "Menü schließen",
diff --git a/public/locales/en-US/grafana.json b/public/locales/en-US/grafana.json
index 33ef5f29eaf..79923a71a71 100644
--- a/public/locales/en-US/grafana.json
+++ b/public/locales/en-US/grafana.json
@@ -935,7 +935,8 @@
     },
     "megamenu": {
       "close": "Close menu",
-      "dock": "Dock menu"
+      "dock": "Dock menu",
+      "undock": "Undock menu"
     },
     "toolbar": {
       "close-menu": "Close menu",
diff --git a/public/locales/es-ES/grafana.json b/public/locales/es-ES/grafana.json
index c79d6c2442e..2ec04f36b0c 100644
--- a/public/locales/es-ES/grafana.json
+++ b/public/locales/es-ES/grafana.json
@@ -941,7 +941,8 @@
     },
     "megamenu": {
       "close": "Cerrar menú",
-      "dock": "Menú base"
+      "dock": "Menú base",
+      "undock": ""
     },
     "toolbar": {
       "close-menu": "Cerrar menú",
diff --git a/public/locales/fr-FR/grafana.json b/public/locales/fr-FR/grafana.json
index bd64c9a5295..fd75a0e3af4 100644
--- a/public/locales/fr-FR/grafana.json
+++ b/public/locales/fr-FR/grafana.json
@@ -941,7 +941,8 @@
     },
     "megamenu": {
       "close": "Fermer le menu",
-      "dock": "Ancrer le menu"
+      "dock": "Ancrer le menu",
+      "undock": ""
     },
     "toolbar": {
       "close-menu": "Fermer le menu",
diff --git a/public/locales/pseudo-LOCALE/grafana.json b/public/locales/pseudo-LOCALE/grafana.json
index 77be386cb16..24d16fe8c07 100644
--- a/public/locales/pseudo-LOCALE/grafana.json
+++ b/public/locales/pseudo-LOCALE/grafana.json
@@ -935,7 +935,8 @@
     },
     "megamenu": {
       "close": "Cľőşę męʼnū",
-      "dock": "Đőčĸ męʼnū"
+      "dock": "Đőčĸ męʼnū",
+      "undock": "Ůʼnđőčĸ męʼnū"
     },
     "toolbar": {
       "close-menu": "Cľőşę męʼnū",
diff --git a/public/locales/zh-Hans/grafana.json b/public/locales/zh-Hans/grafana.json
index a6594545607..f88e92d9fb1 100644
--- a/public/locales/zh-Hans/grafana.json
+++ b/public/locales/zh-Hans/grafana.json
@@ -929,7 +929,8 @@
     },
     "megamenu": {
       "close": "关闭菜单",
-      "dock": "停靠菜单"
+      "dock": "停靠菜单",
+      "undock": ""
     },
     "toolbar": {
       "close-menu": "关闭菜单",