diff --git a/packages/react-aria/src/selection/useSelectableCollection.ts b/packages/react-aria/src/selection/useSelectableCollection.ts
index 3b3bb8413db..99a04de7bd3 100644
--- a/packages/react-aria/src/selection/useSelectableCollection.ts
+++ b/packages/react-aria/src/selection/useSelectableCollection.ts
@@ -487,7 +487,11 @@ export function useSelectableCollection(
       ) {
         navigateToKey(manager.lastSelectedKey ?? delegate.getLastKey?.());
       } else {
-        navigateToKey(manager.firstSelectedKey ?? delegate.getFirstKey?.());
+        let firstKey = manager.firstSelectedKey ?? delegate.getFirstKey?.();
+        if (firstKey != null && manager.disabledKeys.has(firstKey)) {
+          firstKey = delegate.getFirstKey?.() ?? null;
+        }
+        navigateToKey(firstKey);
       }
     } else if (scrollRef.current) {
       // Restore the scroll position to what it was before.
@@ -597,7 +601,6 @@ export function useSelectableCollection(
     if (autoFocusRef.current) {
       let focusedKey: Key | null = null;
 
-      // Check focus strategy to determine which item to focus
       if (autoFocus === 'first') {
         focusedKey = delegate.getFirstKey?.() ?? null;
       }
@@ -605,7 +608,6 @@ export function useSelectableCollection(
         focusedKey = delegate.getLastKey?.() ?? null;
       }
 
-      // If there are any selected keys, make the first one the new focus target
       let selectedKeys = manager.selectedKeys;
       if (selectedKeys.size) {
         for (let key of selectedKeys) {
@@ -616,6 +618,36 @@ export function useSelectableCollection(
         }
       }
 
+      let originalStrategyKey = focusedKey;
+      let visitedKeys = new Set<Key>();
+      let foundEnabledKey = false;
+
+      while (focusedKey != null && !manager.canSelectItem(focusedKey)) {
+        if (visitedKeys.has(focusedKey)) {
+          break;
+        }
+        visitedKeys.add(focusedKey);
+
+        let nextKey = delegate.getKeyBelow?.(focusedKey) ?? null;
+
+        if (nextKey == null || nextKey === focusedKey) {
+          break;
+        }
+
+        if (manager.canSelectItem(nextKey)) {
+          focusedKey = nextKey;
+          foundEnabledKey = true;
+          break;
+        }
+
+        focusedKey = nextKey;
+      }
+
+      // If no enabled key was found, restore original key (this may happen if all items are disabled)
+      if (!foundEnabledKey && focusedKey != null && !manager.canSelectItem(focusedKey)) {
+        focusedKey = originalStrategyKey;
+      }
+
       manager.setFocused(true);
       manager.setFocusedKey(focusedKey);
 
@@ -624,7 +656,6 @@ export function useSelectableCollection(
         focusSafely(ref.current);
       }
 
-      // Wait until the collection has items to autofocus.
       if (manager.collection.size > 0) {
         autoFocusRef.current = false;
         didAutoFocusRef.current = true;
diff --git a/packages/react-aria/test/selection/useSelectableCollection.test.js b/packages/react-aria/test/selection/useSelectableCollection.test.js
index b09e54d5c90..554fad452da 100644
--- a/packages/react-aria/test/selection/useSelectableCollection.test.js
+++ b/packages/react-aria/test/selection/useSelectableCollection.test.js
@@ -193,4 +193,21 @@ describe('useSelectableCollection', () => {
       expect(onSelectionChange2).not.toHaveBeenCalled();
     });
   });
+
+  describe('with disabled items boundary keys', () => {
+    it('should automatically focus the first available enabled item on autoFocus mount when leading items are disabled', () => {
+      let {getAllByRole} = render(
+        <List selectionMode="single" autoFocus="first" disabledKeys={['i1']}>
+          <Item key="i1">Disabled Absolute First Item</Item>
+          <Item key="i2">First Enabled Item</Item>
+          <Item key="i3">Second Enabled Item</Item>
+        </List>
+      );
+
+      let options = getAllByRole('option');
+
+      expect(document.activeElement).toBe(options[1]);
+      expect(options[1].textContent).toBe('First Enabled Item');
+    });
+  });
 });