diff --git a/packages/@react-aria/selection/src/useSelectableCollection.ts b/packages/@react-aria/selection/src/useSelectableCollection.ts
index 16dddf08820..2b9f8a60a91 100644
--- a/packages/@react-aria/selection/src/useSelectableCollection.ts
+++ b/packages/@react-aria/selection/src/useSelectableCollection.ts
@@ -13,7 +13,7 @@
 import {FocusEvent, HTMLAttributes, Key, KeyboardEvent, RefObject, useEffect, useRef} from 'react';
 import {focusSafely, getFocusableTreeWalker} from '@react-aria/focus';
 import {FocusStrategy, KeyboardDelegate} from '@react-types/shared';
-import {focusWithoutScrolling, isMac, mergeProps} from '@react-aria/utils';
+import {focusWithoutScrolling, isMac, mergeProps, useEvent} from '@react-aria/utils';
 import {MultipleSelectionManager} from '@react-stately/selection';
 import {useLocale} from '@react-aria/i18n';
 import {useTypeSelect} from './useTypeSelect';
@@ -264,6 +264,15 @@ export function useSelectableCollection(options: SelectableCollectionOptions): S
     }
   };
 
+  // Store the scroll position so we can restore it later.
+  let scrollPos = useRef({top: 0, left: 0});
+  useEvent(scrollRef, 'scroll', isVirtualized ? null : () => {
+    scrollPos.current = {
+      top: scrollRef.current.scrollTop,
+      left: scrollRef.current.scrollLeft
+    };
+  });
+
   let onFocus = (e: FocusEvent) => {
     if (manager.isFocused) {
       // If a focus event bubbled through a portal, reset focus state.
@@ -291,6 +300,18 @@ export function useSelectableCollection(options: SelectableCollectionOptions): S
       } else {
         manager.setFocusedKey(manager.firstSelectedKey ?? delegate.getFirstKey());
       }
+    } else if (!isVirtualized) {
+      // Restore the scroll position to what it was before.
+      scrollRef.current.scrollTop = scrollPos.current.top;
+      scrollRef.current.scrollLeft = scrollPos.current.left;
+
+      // Refocus and scroll the focused item into view if it exists within the scrollable region.
+      let element = scrollRef.current.querySelector(`[data-key="${manager.focusedKey}"]`) as HTMLElement;
+      if (element) {
+        // This prevents a flash of focus on the first/last element in the collection
+        focusWithoutScrolling(element);
+        scrollIntoView(scrollRef.current, element);
+      }
     }
   };
 
diff --git a/packages/@react-aria/sidenav/test/useSideNav.test.js b/packages/@react-aria/sidenav/test/useSideNav.test.js
index 43f3ed81dbe..7eba4ea7208 100644
--- a/packages/@react-aria/sidenav/test/useSideNav.test.js
+++ b/packages/@react-aria/sidenav/test/useSideNav.test.js
@@ -20,9 +20,15 @@ describe('useSideNav', function () {
   let mockLayout = new ListLayout({
     rowHeight: 40
   });
+  let mockRef = {
+    current: {
+      addEventListener: () => jest.fn(),
+      removeEventListener: () => jest.fn()
+    }
+  };
 
   let renderSideNavHook = (menuProps) => {
-    let {result} = renderHook(() => useSideNav({...menuProps, layout: mockLayout}, mockState));
+    let {result} = renderHook(() => useSideNav({...menuProps, layout: mockLayout}, mockState, mockRef));
     return result.current;
   };