diff --git a/goldens/aria/private/index.api.md b/goldens/aria/private/index.api.md
index 2c0f92483ac2..68bd33a35950 100644
--- a/goldens/aria/private/index.api.md
+++ b/goldens/aria/private/index.api.md
@@ -87,7 +87,7 @@ export class ComboboxPattern {
     readonly isEditable: _angular_core.Signal<boolean>;
     readonly isExpanded: _angular_core.Signal<boolean>;
     readonly isFocused: _angular_core.WritableSignal<boolean>;
-    readonly keyboardEventRelay: _angular_core.WritableSignal<KeyboardEvent | undefined>;
+    readonly keyboardEventRelay: _angular_core.WritableSignal<KeyboardEvent[]>;
     keyboardEventRelayEffect(): void;
     keydown: _angular_core.Signal<KeyboardEventManager<KeyboardEvent>>;
     readonly nativeDisabled: _angular_core.Signal<"" | null>;
diff --git a/src/aria/combobox/combobox.spec.ts b/src/aria/combobox/combobox.spec.ts
index fd10570dfc27..d43fa0b044f6 100644
--- a/src/aria/combobox/combobox.spec.ts
+++ b/src/aria/combobox/combobox.spec.ts
@@ -206,6 +206,42 @@ describe('Combobox', () => {
           options[options.length - 1].id,
         );
       });
+
+      it('should handle multiple navigation keys pressed back to back in the same render', async () => {
+        await down(); // Open popup (focuses options[0]: Alabama)
+
+        dispatchKeyboardEvent(inputElement, 'keydown', undefined, 'ArrowDown');
+        dispatchKeyboardEvent(inputElement, 'keydown', undefined, 'ArrowDown');
+        dispatchKeyboardEvent(inputElement, 'keydown', undefined, 'ArrowDown');
+        await fixture.whenStable();
+
+        const options = getOptions();
+        expect(inputElement.getAttribute('aria-activedescendant')).toBe(options[3].id);
+      });
+
+      it('should handle navigation keys pressed in the same render that opens the popup', async () => {
+        await focus();
+
+        dispatchKeyboardEvent(inputElement, 'keydown', undefined, 'ArrowDown'); // Open (focuses options[0])
+        dispatchKeyboardEvent(inputElement, 'keydown', undefined, 'ArrowDown'); // Move to options[1]
+        await fixture.whenStable();
+
+        const options = getOptions();
+        expect(inputElement.getAttribute('aria-activedescendant')).toBe(options[1].id);
+      });
+
+      it('should relay back-to-back typeahead characters in order on a non-editable combobox', async () => {
+        await setupCombobox(ComboboxSelectOnlyListboxExample);
+        await down(); // Open popup (focuses options[0]: Alabama)
+
+        for (const char of 'new y') {
+          dispatchKeyboardEvent(inputElement, 'keydown', undefined, char);
+        }
+        await fixture.whenStable();
+
+        const newYork = getOption('New York')!;
+        expect(inputElement.getAttribute('aria-activedescendant')).toBe(newYork.id);
+      });
     });
 
     describe('Expansion', () => {
@@ -346,6 +382,18 @@ describe('Combobox', () => {
 
           expect(fixture.componentInstance.valueChanges).toEqual([]);
         });
+
+        it('should select the target option when navigation keys and Enter are pressed in the same render', async () => {
+          await down(); // Open popup (focuses Alabama)
+
+          dispatchKeyboardEvent(inputElement, 'keydown', undefined, 'ArrowDown');
+          dispatchKeyboardEvent(inputElement, 'keydown', undefined, 'ArrowDown');
+          dispatchKeyboardEvent(inputElement, 'keydown', undefined, 'Enter');
+          await fixture.whenStable();
+
+          expect(fixture.componentInstance.value()).toEqual(['Arizona']);
+          expect(inputElement.value).toBe('Arizona');
+        });
       });
 
       describe('with auto-select behavior', () => {
@@ -1937,3 +1985,34 @@ class ComboboxListboxGeneratedIdExample {
   popupExpanded = signal(false);
   options = ['Apple', 'Banana'];
 }
+
+@Component({
+  template: `
+<div>
+  <div
+    ngCombobox
+    #combobox="ngCombobox"
+    aria-label="State"
+    [(expanded)]="popupExpanded"
+  >Pick a state</div>
+
+  <ng-template ngComboboxPopup [combobox]="combobox">
+    <div
+      ngComboboxWidget
+      #listbox="ngListbox"
+      ngListbox
+      focusMode="activedescendant"
+      [activeDescendant]="listbox.activeDescendant()">
+      @for (option of options; track option) {
+        <div ngOption [value]="option" [label]="option">{{option}}</div>
+      }
+    </div>
+  </ng-template>
+</div>
+  `,
+  imports: [Combobox, ComboboxPopup, ComboboxWidget, Listbox, Option],
+})
+class ComboboxSelectOnlyListboxExample {
+  popupExpanded = signal(false);
+  options = states;
+}
diff --git a/src/aria/private/combobox/combobox.spec.ts b/src/aria/private/combobox/combobox.spec.ts
index 471a9cc91fdc..c3ca733fafb7 100644
--- a/src/aria/private/combobox/combobox.spec.ts
+++ b/src/aria/private/combobox/combobox.spec.ts
@@ -273,12 +273,12 @@ describe('ComboboxPattern', () => {
       const shiftUp = createKeyboardEvent('keydown', 38, 'ArrowUp');
       Object.defineProperty(shiftUp, 'shiftKey', {value: true});
       pattern.onKeydown(shiftUp);
-      expect(pattern.keyboardEventRelay()).toBe(shiftUp);
+      expect(pattern.keyboardEventRelay()).toEqual([shiftUp]);
 
       const shiftDown = createKeyboardEvent('keydown', 40, 'ArrowDown');
       Object.defineProperty(shiftDown, 'shiftKey', {value: true});
       pattern.onKeydown(shiftDown);
-      expect(pattern.keyboardEventRelay()).toBe(shiftDown);
+      expect(pattern.keyboardEventRelay()).toEqual([shiftUp, shiftDown]);
     });
 
     it('should NOT forward Ctrl+A or Shift+Home/End for editable inputs', () => {
@@ -288,12 +288,12 @@ describe('ComboboxPattern', () => {
       const ctrlA = createKeyboardEvent('keydown', 65, 'a');
       Object.defineProperty(ctrlA, 'ctrlKey', {value: true});
       pattern.onKeydown(ctrlA);
-      expect(pattern.keyboardEventRelay()).toBeUndefined();
+      expect(pattern.keyboardEventRelay()).toEqual([]);
 
       const shiftHome = createKeyboardEvent('keydown', 36, 'Home');
       Object.defineProperty(shiftHome, 'shiftKey', {value: true});
       pattern.onKeydown(shiftHome);
-      expect(pattern.keyboardEventRelay()).toBeUndefined();
+      expect(pattern.keyboardEventRelay()).toEqual([]);
     });
 
     it('should forward Ctrl+A and Shift+Home/End for select-only (non-editable) comboboxes', () => {
@@ -305,12 +305,23 @@ describe('ComboboxPattern', () => {
       const ctrlA = createKeyboardEvent('keydown', 65, 'a');
       Object.defineProperty(ctrlA, 'ctrlKey', {value: true});
       pattern.onKeydown(ctrlA);
-      expect(pattern.keyboardEventRelay()).toBe(ctrlA);
+      expect(pattern.keyboardEventRelay()).toEqual([ctrlA]);
 
       const shiftHome = createKeyboardEvent('keydown', 36, 'Home');
       Object.defineProperty(shiftHome, 'shiftKey', {value: true});
       pattern.onKeydown(shiftHome);
-      expect(pattern.keyboardEventRelay()).toBe(shiftHome);
+      expect(pattern.keyboardEventRelay()).toEqual([ctrlA, shiftHome]);
+    });
+
+    it('should only enqueue Space once on select-only (non-editable) comboboxes', () => {
+      const selectOnlyElement = document.createElement('div');
+      const {pattern, expanded} = setup();
+      pattern.inputs.element = signal(selectOnlyElement);
+      expanded.set(true);
+
+      const space = createKeyboardEvent('keydown', 32, ' ');
+      pattern.onKeydown(space);
+      expect(pattern.keyboardEventRelay()).toEqual([space]);
     });
   });
 
diff --git a/src/aria/private/combobox/combobox.ts b/src/aria/private/combobox/combobox.ts
index 4e23acbc1c2b..4335cd58fa3d 100644
--- a/src/aria/private/combobox/combobox.ts
+++ b/src/aria/private/combobox/combobox.ts
@@ -88,8 +88,8 @@ export class ComboboxPattern {
     return 'none';
   });
 
-  /** A relay for keyboard events to the popup. */
-  readonly keyboardEventRelay = signal<KeyboardEvent | undefined>(undefined);
+  /** A relay queue for keyboard events to the popup. */
+  readonly keyboardEventRelay = signal<KeyboardEvent[]>([]);
 
   /** Whether the combobox is focused. */
   readonly isFocused = signal(false);
@@ -137,44 +137,43 @@ export class ComboboxPattern {
       .on(
         'ArrowLeft',
         e => {
-          this.keyboardEventRelay.set(e);
+          this._relayKeydown(e);
         },
         {preventDefault: this.popupType() !== 'listbox', ignoreRepeat: false},
       )
       .on(
         'ArrowRight',
         e => {
-          this.keyboardEventRelay.set(e);
+          this._relayKeydown(e);
         },
         {preventDefault: this.popupType() !== 'listbox', ignoreRepeat: false},
       )
-      .on('ArrowUp', e => this.keyboardEventRelay.set(e), {ignoreRepeat: false})
-      .on('ArrowDown', e => this.keyboardEventRelay.set(e), {ignoreRepeat: false})
-      .on(Modifier.Shift, 'ArrowUp', e => this.keyboardEventRelay.set(e), {ignoreRepeat: false})
-      .on(Modifier.Shift, 'ArrowDown', e => this.keyboardEventRelay.set(e), {ignoreRepeat: false})
-      .on('Home', e => this.keyboardEventRelay.set(e))
-      .on('End', e => this.keyboardEventRelay.set(e))
-      .on('PageUp', e => this.keyboardEventRelay.set(e))
-      .on('PageDown', e => this.keyboardEventRelay.set(e))
+      .on('ArrowUp', e => this._relayKeydown(e), {ignoreRepeat: false})
+      .on('ArrowDown', e => this._relayKeydown(e), {ignoreRepeat: false})
+      .on(Modifier.Shift, 'ArrowUp', e => this._relayKeydown(e), {ignoreRepeat: false})
+      .on(Modifier.Shift, 'ArrowDown', e => this._relayKeydown(e), {ignoreRepeat: false})
+      .on('Home', e => this._relayKeydown(e))
+      .on('End', e => this._relayKeydown(e))
+      .on('PageUp', e => this._relayKeydown(e))
+      .on('PageDown', e => this._relayKeydown(e))
       .on('Escape', () => {
         if (!this.inputs.alwaysExpanded()) {
           this.inputs.expanded.set(false);
+          this.keyboardEventRelay.set([]);
         }
       });
 
     if (!this.readonly()) {
-      manager.on('Enter', e => this.keyboardEventRelay.set(e));
+      manager.on('Enter', e => this._relayKeydown(e));
     }
 
     if (!this.isEditable() && !this.readonly()) {
       manager
-        .on(' ', e => this.keyboardEventRelay.set(e))
-        .on([Modifier.Ctrl, Modifier.Meta], 'a', e => this.keyboardEventRelay.set(e))
-        .on([Modifier.Ctrl, Modifier.Meta], 'A', e => this.keyboardEventRelay.set(e))
-        .on(Modifier.Shift, 'Home', e => this.keyboardEventRelay.set(e))
-        .on(Modifier.Shift, 'End', e => this.keyboardEventRelay.set(e))
+        .on([Modifier.Ctrl, Modifier.Meta], 'A', e => this._relayKeydown(e))
+        .on(Modifier.Shift, 'Home', e => this._relayKeydown(e))
+        .on(Modifier.Shift, 'End', e => this._relayKeydown(e))
         .on(/^.$/, e => {
-          this.keyboardEventRelay.set(e);
+          this._relayKeydown(e);
         });
     }
 
@@ -196,6 +195,11 @@ export class ComboboxPattern {
     this.value = inputs.value;
   }
 
+  /** Queues a keyboard event to be relayed to the popup. */
+  private _relayKeydown(event: KeyboardEvent) {
+    this.keyboardEventRelay.update(events => [...events, event]);
+  }
+
   /** Handles keydown events for the combobox. */
   onKeydown(event: KeyboardEvent) {
     if (!this.inputs.disabled()) {
@@ -266,19 +270,24 @@ export class ComboboxPattern {
 
   /** Relays keyboard events to the popup. */
   keyboardEventRelayEffect() {
-    const event = this.keyboardEventRelay();
-    if (event === undefined) return;
+    const events = this.keyboardEventRelay();
+    if (events.length === 0) return;
 
     // Reset isDeleting when the user navigates, so that the highlight effect can run again.
     this.isDeleting.set(false);
 
-    untracked(() => {
-      const popup = this.inputs.popup();
-      if (this.isExpanded()) {
-        const relayedEvent = new KeyboardEvent(event.type, event);
-        popup?.controlTarget()?.dispatchEvent(relayedEvent);
-      }
-    });
+    if (!untracked(() => this.isExpanded())) {
+      this.keyboardEventRelay.set([]);
+      return;
+    }
+
+    const target = this.inputs.popup()?.controlTarget();
+    if (!target) return;
+
+    this.keyboardEventRelay.set([]);
+    for (const event of events) {
+      target.dispatchEvent(new KeyboardEvent(event.type, event));
+    }
   }
 }