diff --git a/goldens/aria/simple-combobox/testing/index.api.md b/goldens/aria/simple-combobox/testing/index.api.md
new file mode 100644
index 000000000000..a9b87fd9d748
--- /dev/null
+++ b/goldens/aria/simple-combobox/testing/index.api.md
@@ -0,0 +1,47 @@
+## API Report File for "@angular/aria_simple-combobox_testing"
+
+> Do not edit this file. It is a report generated by [API Extractor](https://api-extractor.com/).
+
+```ts
+
+import { BaseHarnessFilters } from '@angular/cdk/testing';
+import { ComponentHarness } from '@angular/cdk/testing';
+import { ComponentHarnessConstructor } from '@angular/cdk/testing';
+import { ContentContainerComponentHarness } from '@angular/cdk/testing';
+import { HarnessLoader } from '@angular/cdk/testing';
+import { HarnessPredicate } from '@angular/cdk/testing';
+
+// @public
+export class ComboboxHarness extends ContentContainerComponentHarness {
+    blur(): Promise<void>;
+    close(): Promise<void>;
+    focus(): Promise<void>;
+    getPlaceholder(): Promise<string | null>;
+    getPopupLoader(): Promise<HarnessLoader>;
+    getPopupWidget<T extends ComponentHarness>(type: ComponentHarnessConstructor<T> & {
+        with: (options?: {
+            selector?: string;
+        }) => HarnessPredicate<T>;
+    }): Promise<T>;
+    protected getRootHarnessLoader(): Promise<HarnessLoader>;
+    getValue(): Promise<string>;
+    // (undocumented)
+    static hostSelector: string;
+    isDisabled(): Promise<boolean>;
+    isFocused(): Promise<boolean>;
+    isOpen(): Promise<boolean>;
+    open(): Promise<void>;
+    setValue(value: string): Promise<void>;
+    static with(options?: ComboboxHarnessFilters): HarnessPredicate<ComboboxHarness>;
+}
+
+// @public
+export interface ComboboxHarnessFilters extends BaseHarnessFilters {
+    disabled?: boolean;
+    placeholder?: string | RegExp;
+    value?: string | RegExp;
+}
+
+// (No @packageDocumentation comment for this package)
+
+```
diff --git a/src/aria/config.bzl b/src/aria/config.bzl
index 0e0578591b51..480c93fad6d5 100644
--- a/src/aria/config.bzl
+++ b/src/aria/config.bzl
@@ -10,6 +10,7 @@ ARIA_ENTRYPOINTS = [
     "menu",
     "menu/testing",
     "simple-combobox",
+    "simple-combobox/testing",
     "tabs",
     "tabs/testing",
     "toolbar",
diff --git a/src/aria/simple-combobox/testing/BUILD.bazel b/src/aria/simple-combobox/testing/BUILD.bazel
new file mode 100644
index 000000000000..38540ebe2f98
--- /dev/null
+++ b/src/aria/simple-combobox/testing/BUILD.bazel
@@ -0,0 +1,43 @@
+load("//tools:defaults.bzl", "ng_project", "ng_web_test_suite", "ts_project")
+
+package(default_visibility = ["//visibility:public"])
+
+ts_project(
+    name = "testing",
+    srcs = glob(
+        ["**/*.ts"],
+        exclude = ["**/*.spec.ts"],
+    ),
+    deps = [
+        "//:node_modules/@angular/core",
+        "//src/cdk/testing",
+    ],
+)
+
+filegroup(
+    name = "source-files",
+    srcs = glob(["**/*.ts"]),
+)
+
+ng_project(
+    name = "unit_tests_lib",
+    testonly = True,
+    srcs = glob(["**/*.spec.ts"]),
+    deps = [
+        ":testing",
+        "//:node_modules/@angular/core",
+        "//src/aria/listbox",
+        "//src/aria/listbox/testing",
+        "//src/aria/simple-combobox",
+        "//src/cdk/overlay",
+        "//src/cdk/testing",
+        "//src/cdk/testing/testbed",
+    ],
+)
+
+ng_web_test_suite(
+    name = "unit_tests",
+    deps = [
+        ":unit_tests_lib",
+    ],
+)
diff --git a/src/aria/simple-combobox/testing/combobox-harness-filters.ts b/src/aria/simple-combobox/testing/combobox-harness-filters.ts
new file mode 100644
index 000000000000..22013f276d3d
--- /dev/null
+++ b/src/aria/simple-combobox/testing/combobox-harness-filters.ts
@@ -0,0 +1,19 @@
+/**
+ * @license
+ * Copyright Google LLC All Rights Reserved.
+ *
+ * Use of this source code is governed by an MIT-style license that can be
+ * found in the LICENSE file at https://angular.dev/license
+ */
+
+import {BaseHarnessFilters} from '@angular/cdk/testing';
+
+/** A set of criteria that can be used to filter a list of `ComboboxHarness` instances. */
+export interface ComboboxHarnessFilters extends BaseHarnessFilters {
+  /** Only find instances whose placeholder matches the given value. */
+  placeholder?: string | RegExp;
+  /** Only find instances whose value matches the given value. */
+  value?: string | RegExp;
+  /** Only find instances with the given disabled state. */
+  disabled?: boolean;
+}
diff --git a/src/aria/simple-combobox/testing/combobox-harness.spec.ts b/src/aria/simple-combobox/testing/combobox-harness.spec.ts
new file mode 100644
index 000000000000..8b4ae5351d1a
--- /dev/null
+++ b/src/aria/simple-combobox/testing/combobox-harness.spec.ts
@@ -0,0 +1,200 @@
+/**
+ * @license
+ * Copyright Google LLC All Rights Reserved.
+ *
+ * Use of this source code is governed by an MIT-style license that can be
+ * found in the LICENSE file at https://angular.dev/license
+ */
+
+import {Component, signal} from '@angular/core';
+import {ComponentFixture, TestBed} from '@angular/core/testing';
+import {HarnessLoader} from '@angular/cdk/testing';
+import {TestbedHarnessEnvironment} from '@angular/cdk/testing/testbed';
+import {Combobox, ComboboxPopup, ComboboxWidget} from '../index';
+import {Listbox, Option} from '../../listbox';
+import {ListboxHarness, ListboxOptionHarness} from '../../listbox/testing/listbox-harness';
+import {ComboboxHarness} from './combobox-harness';
+import {OverlayModule} from '@angular/cdk/overlay';
+
+describe('ComboboxHarness', () => {
+  let fixture: ComponentFixture<any>;
+  let loader: HarnessLoader;
+
+  function setupTest(component: any) {
+    fixture = TestBed.createComponent(component);
+    fixture.detectChanges();
+    loader = TestbedHarnessEnvironment.loader(fixture);
+  }
+
+  describe('Basic usage', () => {
+    beforeEach(() => setupTest(ComboboxTestApp));
+
+    it('should load combobox harness', async () => {
+      await expectAsync(loader.getHarness(ComboboxHarness)).toBeResolved();
+    });
+
+    it('should get and set values', async () => {
+      const combobox = await loader.getHarness(ComboboxHarness);
+      await combobox.setValue('California');
+      fixture.detectChanges();
+
+      expect(await combobox.getValue()).toBe('California');
+    });
+
+    it('should correctly report disabled state', async () => {
+      const combobox = await loader.getHarness(ComboboxHarness);
+      expect(await combobox.isDisabled()).toBeFalse();
+
+      fixture.componentInstance.disabled.set(true);
+      fixture.detectChanges();
+
+      expect(await combobox.isDisabled()).toBeTrue();
+    });
+
+    it('should open and close the popup', async () => {
+      const combobox = await loader.getHarness(ComboboxHarness);
+      expect(await combobox.isOpen()).toBeFalse();
+
+      await combobox.open();
+      fixture.detectChanges();
+      expect(await combobox.isOpen()).toBeTrue();
+
+      await combobox.close();
+      fixture.detectChanges();
+      expect(await combobox.isOpen()).toBeFalse();
+    });
+
+    it('should allow loading nested harnesses within the popup content via unified container API', async () => {
+      const combobox = await loader.getHarness(ComboboxHarness);
+      await combobox.open();
+      fixture.detectChanges();
+
+      // We access the main widget harness using getPopupWidget.
+      const listbox = await combobox.getPopupWidget(ListboxHarness);
+      const options = await listbox.getOptions();
+      expect(options.length).toBe(3);
+    });
+
+    it('should fail to resolve nested items when closed', async () => {
+      const combobox = await loader.getHarness(ComboboxHarness);
+      // Popup isn't open yet, so getPopupWidget should fail.
+      await expectAsync(combobox.getPopupWidget(ListboxHarness)).toBeRejectedWithError(
+        /Cannot retrieve popup content because the combobox is closed/,
+      );
+    });
+
+    it('should support getting explicit popup loader for descendant matching', async () => {
+      const combobox = await loader.getHarness(ComboboxHarness);
+      await combobox.open();
+      fixture.detectChanges();
+
+      const popupLoader = await combobox.getPopupLoader();
+      // We are testing that the loader works for finding actual children (Options).
+      const option = await popupLoader.getHarness(ListboxOptionHarness);
+      expect(option).toBeDefined();
+    });
+
+    it('should support focusing and blurring', async () => {
+      const combobox = await loader.getHarness(ComboboxHarness);
+      await combobox.focus();
+      expect(await combobox.isFocused()).toBeTrue();
+
+      await combobox.blur();
+      expect(await combobox.isFocused()).toBeFalse();
+    });
+  });
+
+  describe('Overlay and Popover integrations', () => {
+    it('should find and resolve harnesses nested inside standard CdkOverlay', async () => {
+      setupTest(ComboboxOverlayTestApp);
+      const combobox = await loader.getHarness(ComboboxHarness);
+
+      await combobox.open();
+      fixture.detectChanges();
+
+      // Should find listbox inside the dynamically attached cdk overlay root container
+      const listbox = await combobox.getPopupWidget(ListboxHarness);
+      expect(listbox).toBeDefined();
+      expect((await listbox.getOptions()).length).toBe(2);
+    });
+
+    it('should resolve nested harnesses when using Native Popover API', async () => {
+      setupTest(ComboboxNativePopoverTestApp);
+      const combobox = await loader.getHarness(ComboboxHarness);
+
+      await combobox.open();
+      fixture.detectChanges();
+
+      const listbox = await combobox.getPopupWidget(ListboxHarness);
+      expect(listbox).toBeDefined();
+      expect((await listbox.getOptions()).length).toBe(2);
+    });
+  });
+});
+
+@Component({
+  template: `
+    <div>
+      <input
+        ngCombobox
+        #combobox="ngCombobox"
+        placeholder="Search states"
+        [disabled]="disabled()"
+      />
+
+      <ng-template ngComboboxPopup [combobox]="combobox">
+        <div ngComboboxWidget #listbox="ngListbox" ngListbox id="listbox-widget" focusMode="activedescendant" [activeDescendant]="listbox.activeDescendant()">
+          <div ngOption value="CA" label="California">California</div>
+          <div ngOption value="WA" label="Washington">Washington</div>
+          <div ngOption value="OR" label="Oregon">Oregon</div>
+        </div>
+      </ng-template>
+    </div>
+  `,
+  imports: [Combobox, ComboboxPopup, ComboboxWidget, Listbox, Option],
+})
+class ComboboxTestApp {
+  disabled = signal(false);
+}
+
+@Component({
+  template: `
+    <div #origin>
+      <input ngCombobox #combobox="ngCombobox" [(expanded)]="popupExpanded" />
+    </div>
+
+    <ng-template cdkConnectedOverlay [cdkConnectedOverlayOrigin]="origin" [cdkConnectedOverlayOpen]="popupExpanded()">
+      <ng-template ngComboboxPopup [combobox]="combobox">
+        <div ngComboboxWidget ngListbox id="overlay-listbox">
+          <div ngOption value="A">A</div>
+          <div ngOption value="B">B</div>
+        </div>
+      </ng-template>
+    </ng-template>
+  `,
+  imports: [Combobox, ComboboxPopup, ComboboxWidget, Listbox, Option, OverlayModule],
+})
+class ComboboxOverlayTestApp {
+  popupExpanded = signal(false);
+}
+
+@Component({
+  template: `
+    <div #origin>
+      <input ngCombobox #combobox="ngCombobox" [(expanded)]="popupExpanded" />
+    </div>
+
+    <ng-template [cdkConnectedOverlay]="{origin, usePopover: 'inline'}" [cdkConnectedOverlayOpen]="popupExpanded()">
+      <ng-template ngComboboxPopup [combobox]="combobox">
+        <div ngComboboxWidget ngListbox id="popover-listbox">
+          <div ngOption value="A">A</div>
+          <div ngOption value="B">B</div>
+        </div>
+      </ng-template>
+    </ng-template>
+  `,
+  imports: [Combobox, ComboboxPopup, ComboboxWidget, Listbox, Option, OverlayModule],
+})
+class ComboboxNativePopoverTestApp {
+  popupExpanded = signal(false);
+}
diff --git a/src/aria/simple-combobox/testing/combobox-harness.ts b/src/aria/simple-combobox/testing/combobox-harness.ts
new file mode 100644
index 000000000000..c13a53b69634
--- /dev/null
+++ b/src/aria/simple-combobox/testing/combobox-harness.ts
@@ -0,0 +1,151 @@
+/**
+ * @license
+ * Copyright Google LLC All Rights Reserved.
+ *
+ * Use of this source code is governed by an MIT-style license that can be
+ * found in the LICENSE file at https://angular.dev/license
+ */
+
+import {
+  ComponentHarness,
+  ComponentHarnessConstructor,
+  ContentContainerComponentHarness,
+  HarnessLoader,
+  HarnessPredicate,
+  TestKey,
+} from '@angular/cdk/testing';
+import {ComboboxHarnessFilters} from './combobox-harness-filters';
+
+/** Harness for interacting with a standard `ngCombobox` input element in tests. */
+export class ComboboxHarness extends ContentContainerComponentHarness {
+  static hostSelector = '[ngCombobox]';
+
+  /**
+   * Gets a `HarnessPredicate` that can be used to search for a combobox with specific attributes.
+   * @param options Options for filtering which combobox instances are considered a match.
+   * @return a `HarnessPredicate` configured with the given options.
+   */
+  static with(options: ComboboxHarnessFilters = {}): HarnessPredicate<ComboboxHarness> {
+    return new HarnessPredicate(ComboboxHarness, options)
+      .addOption('placeholder', options.placeholder, async (harness, placeholder) =>
+        HarnessPredicate.stringMatches(await harness.getPlaceholder(), placeholder),
+      )
+      .addOption('value', options.value, async (harness, value) =>
+        HarnessPredicate.stringMatches(await harness.getValue(), value),
+      )
+      .addOption(
+        'disabled',
+        options.disabled,
+        async (harness, disabled) => (await harness.isDisabled()) === disabled,
+      );
+  }
+
+  /**
+   * Gets the component harness for the active widget contained inside the popup.
+   * Use this when you need to access the harness of the widget itself (e.g., `ListboxHarness`),
+   * rather than querying items within it.
+   * @param type The harness type to locate. Must implement standard static `.with()` method.
+   */
+  async getPopupWidget<T extends ComponentHarness>(
+    type: ComponentHarnessConstructor<T> & {
+      with: (options?: {selector?: string}) => HarnessPredicate<T>;
+    },
+  ): Promise<T> {
+    const host = await this.host();
+    const controlsId = await host.getAttribute('aria-controls');
+    if (!controlsId) {
+      throw new Error(
+        'Cannot retrieve popup content because the combobox is closed or not associated with a popup controls ID.',
+      );
+    }
+    return this.documentRootLocatorFactory().locatorFor(type.with({selector: `#${controlsId}`}))();
+  }
+
+  /**
+   * Gets a harness loader scoped to the content inside the popup container.
+   * Note that lookups performed by this loader will only find descendants of the popup container.
+   */
+  async getPopupLoader(): Promise<HarnessLoader> {
+    return this.getRootHarnessLoader();
+  }
+
+  /** Overrides root loader to automatically resolve queries nested inside the associated popup. */
+  protected override async getRootHarnessLoader(): Promise<HarnessLoader> {
+    const host = await this.host();
+    const controlsId = await host.getAttribute('aria-controls');
+    if (!controlsId) {
+      throw new Error(
+        'Cannot retrieve popup content because the combobox is closed or not associated with a popup controls ID.',
+      );
+    }
+    const documentRoot = await this.documentRootLocatorFactory().rootHarnessLoader();
+    // Locate the widget by ID, which was assigned by ngComboboxWidget and linked via aria-controls.
+    return documentRoot.getChildLoader(`#${controlsId}`);
+  }
+
+  /** Whether the combobox is expanded (popup is open). */
+  async isOpen(): Promise<boolean> {
+    const host = await this.host();
+    return (await host.getAttribute('aria-expanded')) === 'true';
+  }
+
+  /** Whether the combobox is disabled. */
+  async isDisabled(): Promise<boolean> {
+    const host = await this.host();
+    return (await host.getAttribute('aria-disabled')) === 'true';
+  }
+
+  /** Gets the current value string of the combobox input. */
+  async getValue(): Promise<string> {
+    const host = await this.host();
+    return host.getProperty<string>('value');
+  }
+
+  /** Sets the value of the combobox input. */
+  async setValue(value: string): Promise<void> {
+    const host = await this.host();
+    await host.clear();
+    if (value) {
+      await host.sendKeys(value);
+    }
+  }
+
+  /** Gets the placeholder text of the combobox. */
+  async getPlaceholder(): Promise<string | null> {
+    const host = await this.host();
+    return host.getAttribute('placeholder');
+  }
+
+  /** Opens the combobox popup if it is currently closed. */
+  async open(): Promise<void> {
+    if (!(await this.isOpen())) {
+      const host = await this.host();
+      await host.focus();
+      await host.sendKeys(TestKey.DOWN_ARROW);
+    }
+  }
+
+  /** Closes the combobox popup if it is currently open. */
+  async close(): Promise<void> {
+    if (await this.isOpen()) {
+      const host = await this.host();
+      await host.focus();
+      await host.sendKeys(TestKey.ESCAPE);
+    }
+  }
+
+  /** Focuses the combobox. */
+  async focus(): Promise<void> {
+    return (await this.host()).focus();
+  }
+
+  /** Blurs the combobox. */
+  async blur(): Promise<void> {
+    return (await this.host()).blur();
+  }
+
+  /** Whether the combobox has focus. */
+  async isFocused(): Promise<boolean> {
+    return (await this.host()).isFocused();
+  }
+}
diff --git a/src/aria/simple-combobox/testing/index.ts b/src/aria/simple-combobox/testing/index.ts
new file mode 100644
index 000000000000..52b3c7a5156f
--- /dev/null
+++ b/src/aria/simple-combobox/testing/index.ts
@@ -0,0 +1,9 @@
+/**
+ * @license
+ * Copyright Google LLC All Rights Reserved.
+ *
+ * Use of this source code is governed by an MIT-style license that can be
+ * found in the LICENSE file at https://angular.dev/license
+ */
+
+export * from './public-api';
diff --git a/src/aria/simple-combobox/testing/public-api.ts b/src/aria/simple-combobox/testing/public-api.ts
new file mode 100644
index 000000000000..46b2e5953146
--- /dev/null
+++ b/src/aria/simple-combobox/testing/public-api.ts
@@ -0,0 +1,10 @@
+/**
+ * @license
+ * Copyright Google LLC All Rights Reserved.
+ *
+ * Use of this source code is governed by an MIT-style license that can be
+ * found in the LICENSE file at https://angular.dev/license
+ */
+
+export * from './combobox-harness';
+export * from './combobox-harness-filters';