diff --git a/packages/react-aria/src/focus/FocusScope.tsx b/packages/react-aria/src/focus/FocusScope.tsx
index ad4f0a427a3..41114eeadcf 100644
--- a/packages/react-aria/src/focus/FocusScope.tsx
+++ b/packages/react-aria/src/focus/FocusScope.tsx
@@ -538,7 +538,7 @@ function focusElement(element: FocusableElement | null, scroll = false) {
   }
 }
 
-function getFirstInScope(scope: Element[], tabbable = true) {
+function getFirstInScope(scope: Element[], tabbable = true): FocusableElement | null {
   let sentinel = scope[0].previousElementSibling!;
   let scopeRoot = getScopeRoot(scope);
   let walker = getFocusableTreeWalker(scopeRoot, {tabbable}, scope);
@@ -553,7 +553,8 @@ function getFirstInScope(scope: Element[], tabbable = true) {
     nextNode = walker.nextNode();
   }
 
-  return nextNode as FocusableElement;
+  // TreeWalker.nextNode() returns null when the scope contains no focusable element.
+  return nextNode as FocusableElement | null;
 }
 
 function focusFirstInScope(scope: Element[], tabbable: boolean = true) {
@@ -811,8 +812,12 @@ function useRestoreFocus(
               ) {
                 // oxlint-disable-next-line react-hooks/exhaustive-deps
                 let node = getFirstInScope(treeNode.scopeRef.current, true);
-                restoreFocusToElement(node);
-                return;
+                // The scope may have nothing focusable in it, e.g. if its focusable
+                // content was removed or hidden. Keep walking up in that case.
+                if (node) {
+                  restoreFocusToElement(node);
+                  return;
+                }
               }
               treeNode = treeNode.parent;
             }
diff --git a/packages/react-aria/test/focus/FocusScope.test.js b/packages/react-aria/test/focus/FocusScope.test.js
index 39dd0d8be39..e5c3a50b3b2 100644
--- a/packages/react-aria/test/focus/FocusScope.test.js
+++ b/packages/react-aria/test/focus/FocusScope.test.js
@@ -2096,6 +2096,52 @@ describe('FocusScope', function () {
     });
   });
   describe('node to restore edge cases', () => {
+    it('does not throw when there is no focusable element to restore focus to', function () {
+      function Test({show, showRestoreTarget}) {
+        return (
+          // The outer scope stays mounted and always contains the wrapper div, so
+          // it is never an empty scope, but once showRestoreTarget is false it
+          // holds no focusable element for the restore fallback to find.
+          <FocusScope>
+            <div>
+              {showRestoreTarget && <button data-testid="restore-target">restore target</button>}
+            </div>
+            {show && (
+              <FocusScope restoreFocus autoFocus>
+                <button data-testid="inside">inside</button>
+              </FocusScope>
+            )}
+          </FocusScope>
+        );
+      }
+
+      let {getByTestId, rerender} = render(<Test show={false} showRestoreTarget />);
+      let restoreTarget = getByTestId('restore-target');
+      act(() => {
+        restoreTarget.focus();
+      });
+      expect(document.activeElement).toBe(restoreTarget);
+
+      // Mount the restoreFocus scope. autoFocus moves focus inside it, and the
+      // restore target is captured as its nodeToRestore.
+      rerender(<Test show showRestoreTarget />);
+      act(() => {
+        jest.runAllTimers();
+      });
+      expect(document.activeElement).toBe(getByTestId('inside'));
+
+      // Unmount the scope and remove the restore target in the same commit, so
+      // nodeToRestore is disconnected and the fallback walks up to the outer
+      // scope, which now has nothing focusable in it.
+      rerender(<Test show={false} showRestoreTarget={false} />);
+      act(() => {
+        jest.runAllTimers();
+      });
+
+      // There was nothing to restore to, so focus is left on the body.
+      expect(document.activeElement).toBe(document.body);
+    });
+
     it('tracks node to restore if the node to restore was removed in another part of the tree', async () => {
       function Test() {
         let [showMenu, setShowMenu] = useState(false);