diff --git a/docs/config/browser/expect.md b/docs/config/browser/expect.md
index 45c3a21a3..42580174c 100644
--- a/docs/config/browser/expect.md
+++ b/docs/config/browser/expect.md
@@ -46,10 +46,19 @@ export default defineConfig({
 can be configured here. Additionally, two path resolution functions are
 available: `resolveScreenshotPath` and `resolveDiffPath`.
 
+## browser.expect.toMatchScreenshot.screenshotDirectory
+
+- **Type:** `string | undefined`
+- **Default:** `__screenshots__`
+
+The directory name used for storing reference screenshots.
+
+This value is passed as `screenshotDirectory` to [`browser.expect.toMatchScreenshot.resolveScreenshotPath`](#browserexpecttomatchscreenshotresolvescreenshotpath) and [`browser.expect.toMatchScreenshot.resolveDiffPath`](#browserexpecttomatchscreenshotresolvediffpath), and used in the default path resolution of `resolveScreenshotPath`.
+
 ## browser.expect.toMatchScreenshot.resolveScreenshotPath
 
 - **Type:** `(data: PathResolveData) => string`
-- **Default output:** `` `${root}/${testFileDirectory}/${screenshotDirectory}/${testFileName}/${arg}-${browserName}-${platform}${ext}` ``
+- **Default output:** ``path.resolve(root, testFileDirectory, screenshotDirectory, testFileName, `${arg}-${browserName}-${platform}${ext}`)``
 
 A function to customize where reference screenshots are stored. The function
 receives an object with the following properties:
@@ -92,9 +101,7 @@ receives an object with the following properties:
 
 - `screenshotDirectory: string`
 
-  The value provided to
-  [`browser.screenshotDirectory`](/config/browser/screenshotdirectory),
-  if none is provided, its default value.
+  The value provided to [`browser.expect.toMatchScreenshot.screenshotDirectory`](#browserexpecttomatchscreenshotscreenshotdirectory), if none is provided, its default value (`__screenshots__`).
 
 - `root: string`
 
@@ -132,7 +139,7 @@ resolveScreenshotPath: ({ arg, browserName, ext, root, testFileName }) =>
 ## browser.expect.toMatchScreenshot.resolveDiffPath
 
 - **Type:** `(data: PathResolveData) => string`
-- **Default output:** `` `${root}/${attachmentsDir}/${testFileDirectory}/${testFileName}/${arg}-${browserName}-${platform}${ext}` ``
+- **Default output:** ``path.resolve(root, attachmentsDir, testFileDirectory, testFileName, `${arg}-${browserName}-${platform}${ext}`)``
 
 A function to customize where diff images are stored when screenshot comparisons
 fail. Receives the same data object as
diff --git a/docs/guide/migration.md b/docs/guide/migration.md
index 73b91fb56..10e60690e 100644
--- a/docs/guide/migration.md
+++ b/docs/guide/migration.md
@@ -182,6 +182,32 @@ Vitest now uses a single `.vitest` directory at the project root as the shared a
 - **Blob reporter** and `--merge-reports`: `.vitest-reports/blob-*.json` → `.vitest/blob/blob-*.json`
 - **HTML reporter** ([`html`](/guide/reporters#html-reporter)): `html/index.html` → `.vitest/index.html`, and its option changed from `outputFile` (a file) to `outputDir` (a directory)
 
+### `toMatchScreenshot` Now Uses a Dedicated Screenshot Directory Config
+
+Previously, reference screenshots for `toMatchScreenshot` did not correctly respect `browser.screenshotDirectory`. As a result, screenshots were saved in an unintended location when a custom directory was configured.
+
+This has now been fixed by introducing a dedicated option: `browser.expect.toMatchScreenshot.screenshotDirectory`. Its default value is `__screenshots__`.
+
+- If you did not set `browser.screenshotDirectory`, no changes are required.
+- If you did set `browser.screenshotDirectory`, you must now explicitly configure the new option:
+
+    ```ts [vitest.config.ts]
+    export default defineConfig({
+      test: {
+        browser: {
+          screenshotDirectory: 'my-screenshots',
+          expect: { // [!code ++]
+            toMatchScreenshot: { // [!code ++]
+              screenshotDirectory: 'my-screenshots', // [!code ++]
+            }, // [!code ++]
+          }, // [!code ++]
+        },
+      },
+    })
+    ```
+
+    Then either move existing reference screenshots to the new location or regenerate them.
+
 ## Migrating to Vitest 4.0 {#vitest-4}
 
 ::: warning Prerequisites
diff --git a/packages/browser/src/node/commands/screenshotMatcher/utils.ts b/packages/browser/src/node/commands/screenshotMatcher/utils.ts
index 242f8aed3..2b60575c0 100644
--- a/packages/browser/src/node/commands/screenshotMatcher/utils.ts
+++ b/packages/browser/src/node/commands/screenshotMatcher/utils.ts
@@ -17,7 +17,7 @@ type GlobalOptions = Required<Omit<
     NonNullable<BrowserConfigOptions['expect']>['toMatchScreenshot']
     & NonNullable<Pick<ScreenshotMatcherArguments[2], 'screenshotOptions'>>
   >,
-  'comparators'
+  'comparators' | 'screenshotDirectory'
 >>
 
 const defaultOptions = {
@@ -135,10 +135,7 @@ export function resolveOptions(
     ext: `.${extension}`,
     platform: platform(),
     root,
-    screenshotDirectory: relative(
-      root,
-      join(root, context.project.config.browser.screenshotDirectory ?? '__screenshots__'),
-    ),
+    screenshotDirectory: context.project.config.browser.expect?.toMatchScreenshot?.screenshotDirectory ?? '__screenshots__',
     attachmentsDir: relative(root, context.project.config.attachmentsDir),
     testFileDirectory: relative(root, dirname(context.testPath)),
     testFileName: basename(context.testPath),
diff --git a/packages/vitest/src/node/types/browser.ts b/packages/vitest/src/node/types/browser.ts
index 06ef6c766..c18edee66 100644
--- a/packages/vitest/src/node/types/browser.ts
+++ b/packages/vitest/src/node/types/browser.ts
@@ -518,9 +518,7 @@ type ToMatchScreenshotResolvePath = (data: {
    */
   platform: NodeJS.Platform
   /**
-   * The value provided to
-   * {@linkcode https://vitest.dev/config/browser/screenshotdirectory|browser.screenshotDirectory},
-   * if none is provided, its default value.
+   * The value provided to {@linkcode ToMatchScreenshotOptions.screenshotDirectory|browser.expect.toMatchScreenshot.screenshotDirectory}, if none is provided, its default value (`__screenshots__`).
    */
   screenshotDirectory: string
   /**
@@ -557,16 +555,24 @@ type ToMatchScreenshotResolvePath = (data: {
 }) => string
 
 export interface ToMatchScreenshotOptions {
+  /**
+   * The directory name used for storing reference screenshots.
+   *
+   * This value is passed as `screenshotDirectory` to {@linkcode resolveScreenshotPath|browser.expect.toMatchScreenshot.resolveScreenshotPath} and {@linkcode resolveDiffPath|browser.expect.toMatchScreenshot.resolveDiffPath}, and used in the default path resolution of `resolveScreenshotPath`.
+   *
+   * @default `__screenshots__`.
+   */
+  screenshotDirectory?: string
   /**
    * Overrides default reference screenshot path.
    *
-   * @default `${root}/${testFileDirectory}/${screenshotDirectory}/${testFileName}/${arg}-${browserName}-${platform}${ext}`
+   * @default path.resolve(root, testFileDirectory, screenshotDirectory, testFileName, `${arg}-${browserName}-${platform}${ext}`)
    */
   resolveScreenshotPath?: ToMatchScreenshotResolvePath
   /**
    * Overrides default screenshot path used for diffs.
    *
-   * @default `${root}/${attachmentsDir}/${testFileDirectory}/${testFileName}/${arg}-${browserName}-${platform}${ext}`
+   * @default path.resolve(root, attachmentsDir, testFileDirectory, testFileName, `${arg}-${browserName}-${platform}${ext}`)
    */
   resolveDiffPath?: ToMatchScreenshotResolvePath
 }
diff --git a/test/browser/specs/to-match-screenshot.test.ts b/test/browser/specs/to-match-screenshot.test.ts
index d652a1cbe..8843f1e87 100644
--- a/test/browser/specs/to-match-screenshot.test.ts
+++ b/test/browser/specs/to-match-screenshot.test.ts
@@ -131,6 +131,47 @@ describe('--watch', () => {
     },
   )
 
+  test(
+    'uses the `screenshotDirectory` option from config',
+    async () => {
+      const customDir = 'my-screenshots'
+
+      const { stderr } = await runBrowserTests(
+        {
+          [testFilename]: testContent,
+          'utils.ts': utilsContent,
+        },
+        {
+          browser: {
+            enabled: true,
+            screenshotFailures: false,
+            provider,
+            headless: true,
+            instances,
+            viewport: {
+              width: 400,
+              height: 200,
+            },
+            expect: {
+              toMatchScreenshot: {
+                screenshotDirectory: customDir,
+              },
+            },
+          },
+          update: 'new',
+        },
+      )
+
+      const references = extractToMatchScreenshotPaths(stderr, testName)
+
+      expect(references.length).toBeGreaterThan(0)
+
+      for (const referencePath of references) {
+        expect(referencePath).toContain(`/${customDir}/`)
+      }
+    },
+  )
+
   describe('--update', () => {
     test(
       'creates snapshot and does NOT update it if reference matches',