diff --git a/packages/@react-aria/combobox/src/useComboBox.ts b/packages/@react-aria/combobox/src/useComboBox.ts
index 5fe460012f0..cead9d21920 100644
--- a/packages/@react-aria/combobox/src/useComboBox.ts
+++ b/packages/@react-aria/combobox/src/useComboBox.ts
@@ -117,6 +117,7 @@ export function useComboBox<T>(props: AriaComboBoxOptions<T>, state: ComboBoxSta
     keyboardDelegate: delegate,
     disallowTypeAhead: true,
     disallowEmptySelection: true,
+    autoFocus: 'first',
     shouldFocusWrap,
     ref: inputRef,
     // Prevent item scroll behavior from being applied here, should be handled in the user's Popover + ListBox component
diff --git a/packages/@react-stately/combobox/src/useComboBoxState.ts b/packages/@react-stately/combobox/src/useComboBoxState.ts
index e2cce7de048..ad1ec15027d 100644
--- a/packages/@react-stately/combobox/src/useComboBoxState.ts
+++ b/packages/@react-stately/combobox/src/useComboBoxState.ts
@@ -236,7 +236,10 @@ export function useComboBoxState<T extends object>(props: ComboBoxStateOptions<T
 
     // Clear focused key when input value changes and display filtered collection again.
     if (inputValue !== lastValue) {
-      selectionManager.setFocusedKey(null);
+      const firstKey = filteredCollection.getFirstKey();
+      if (firstKey) {
+        selectionManager.setFocusedKey(firstKey);
+      }
       setShowAllItems(false);
 
       // Set selectedKey to null when the user clears the input.
diff --git a/packages/react-aria-components/src/ComboBox.tsx b/packages/react-aria-components/src/ComboBox.tsx
index 538b381b32a..087bbb256ff 100644
--- a/packages/react-aria-components/src/ComboBox.tsx
+++ b/packages/react-aria-components/src/ComboBox.tsx
@@ -220,7 +220,7 @@ function ComboBoxInner<T extends object>({props, collection, comboBoxRef: ref}:
           style: {'--trigger-width': menuWidth} as React.CSSProperties,
           clearContexts: CLEAR_CONTEXTS
         }],
-        [ListBoxContext, {...listBoxProps, ref: listBoxRef}],
+        [ListBoxContext, {...listBoxProps, autoFocus: 'first', ref: listBoxRef}],
         [ListStateContext, state],
         [TextContext, {
           slots: {