diff --git a/CHANGELOG.md b/CHANGELOG.md
index 67d8a7cd9fc5..8b0ea9c4eec4 100644
--- a/CHANGELOG.md
+++ b/CHANGELOG.md
@@ -12,7 +12,7 @@
 - `[jest-environment-node]` [**BREAKING**] Add default `node` and `node-addon` conditions to `exportConditions` for `node` environment ([#11924](https://github.com/facebook/jest/pull/11924))
 - `[@jest/expect]` New module which extends `expect` with `jest-snapshot` matchers ([#12404](https://github.com/facebook/jest/pull/12404), [#12410](https://github.com/facebook/jest/pull/12410), [#12418](https://github.com/facebook/jest/pull/12418))
 - `[@jest/expect-utils]` New module exporting utils for `expect` ([#12323](https://github.com/facebook/jest/pull/12323))
-- `[jest-resolver]` [**BREAKING**] Add support for `package.json` `exports` ([11961](https://github.com/facebook/jest/pull/11961))
+- `[jest-resolve]` [**BREAKING**] Add support for `package.json` `exports` ([#11961](https://github.com/facebook/jest/pull/11961), [#12373](https://github.com/facebook/jest/pull/12373))
 - `[jest-resolve, jest-runtime]` Add support for `data:` URI import and mock ([#12392](https://github.com/facebook/jest/pull/12392))
 - `[@jest/schemas]` New module for JSON schemas for Jest's config ([#12384](https://github.com/facebook/jest/pull/12384))
 - `[jest-worker]` [**BREAKING**] Allow only absolute `workerPath` ([#12343](https://github.com/facebook/jest/pull/12343))
diff --git a/e2e/runtime-internal-module-registry/__tests__/runtimeInternalModuleRegistry.test.js b/e2e/runtime-internal-module-registry/__tests__/runtimeInternalModuleRegistry.test.js
index 23d7ba831933..53334daccdb5 100644
--- a/e2e/runtime-internal-module-registry/__tests__/runtimeInternalModuleRegistry.test.js
+++ b/e2e/runtime-internal-module-registry/__tests__/runtimeInternalModuleRegistry.test.js
@@ -13,10 +13,10 @@ describe('Runtime internal module registry', () => {
   it('behaves correctly when requiring a module that is used by jest internals', () => {
     const fs = require('fs');
 
-    // We require from this crazy path so that we can mimick Jest (and it's
-    // transitive deps) being installed along side a projects deps (e.g. with an
+    // We require from this crazy path so that we can mimick Jest (and its
+    // transitive deps) being installed alongside a projects deps (e.g. with an
     // NPM3 flat dep tree)
-    const jestUtil = require('../../../packages/jest-util');
+    const jestUtil = require('jest-util');
 
     // If FS is mocked correctly, this folder won't actually be created on the
     // filesystem
diff --git a/packages/jest-resolve/src/__mocks__/conditions/node_modules/exports/package.json b/packages/jest-resolve/src/__mocks__/conditions/node_modules/exports/package.json
index 7fd4bab2a661..fc9039934b2c 100644
--- a/packages/jest-resolve/src/__mocks__/conditions/node_modules/exports/package.json
+++ b/packages/jest-resolve/src/__mocks__/conditions/node_modules/exports/package.json
@@ -11,6 +11,7 @@
     "./deeplyNested" : {
       "require": "./nestedRequire.js",
       "default": "./nestedDefault.js"
-    }
+    },
+    "./directory/*": "./some-other-directory/*"
   }
 }
diff --git a/packages/jest-resolve/src/__mocks__/conditions/node_modules/exports/some-other-directory/file.js b/packages/jest-resolve/src/__mocks__/conditions/node_modules/exports/some-other-directory/file.js
new file mode 100644
index 000000000000..e69de29bb2d1
diff --git a/packages/jest-resolve/src/__tests__/resolve.test.ts b/packages/jest-resolve/src/__tests__/resolve.test.ts
index 6c6dfaf0705e..4d0b1af072a6 100644
--- a/packages/jest-resolve/src/__tests__/resolve.test.ts
+++ b/packages/jest-resolve/src/__tests__/resolve.test.ts
@@ -234,6 +234,20 @@ describe('findNodeModule', () => {
         path.resolve(conditionsRoot, './node_modules/exports/nestedDefault.js'),
       );
     });
+
+    test('supports separate directory path', () => {
+      const result = Resolver.findNodeModule('exports/directory/file.js', {
+        basedir: conditionsRoot,
+        conditions: [],
+      });
+
+      expect(result).toEqual(
+        path.resolve(
+          conditionsRoot,
+          './node_modules/exports/some-other-directory/file.js',
+        ),
+      );
+    });
   });
 });
 
diff --git a/packages/jest-resolve/src/defaultResolver.ts b/packages/jest-resolve/src/defaultResolver.ts
index 1ca6204d0b6d..893a18b1b3bf 100644
--- a/packages/jest-resolve/src/defaultResolver.ts
+++ b/packages/jest-resolve/src/defaultResolver.ts
@@ -5,14 +5,13 @@
  * LICENSE file in the root directory of this source tree.
  */
 
-import {isAbsolute} from 'path';
+import {dirname, isAbsolute, resolve as pathResolve} from 'path';
 import pnpResolver from 'jest-pnp-resolver';
-import {sync as resolveSync} from 'resolve';
+import {SyncOpts as UpstreamResolveOptions, sync as resolveSync} from 'resolve';
 import {
   Options as ResolveExportsOptions,
   resolve as resolveExports,
 } from 'resolve.exports';
-import slash = require('slash');
 import {
   PkgJson,
   isDirectory,
@@ -36,6 +35,9 @@ interface ResolverOptions {
   pathFilter?: (pkg: PkgJson, path: string, relativePath: string) => string;
 }
 
+type UpstreamResolveOptionsWithConditions = UpstreamResolveOptions &
+  Pick<ResolverOptions, 'conditions'>;
+
 // https://github.com/facebook/jest/pull/10617
 declare global {
   namespace NodeJS {
@@ -55,16 +57,22 @@ export default function defaultResolver(
     return pnpResolver(path, options);
   }
 
-  const result = resolveSync(path, {
+  const resolveOptions: UpstreamResolveOptionsWithConditions = {
     ...options,
     isDirectory,
     isFile,
-    packageFilter: createPackageFilter(path, options.packageFilter),
-    pathFilter: createPathFilter(path, options.conditions, options.pathFilter),
     preserveSymlinks: false,
     readPackageSync,
     realpathSync,
-  });
+  };
+
+  const pathToResolve = getPathInModule(path, resolveOptions);
+
+  const result =
+    // if `getPathInModule` doesn't change the path, attempt to resolve it
+    pathToResolve === path
+      ? resolveSync(pathToResolve, resolveOptions)
+      : pathToResolve;
 
   // Dereference symlinks to ensure we don't create a separate
   // module instance depending on how it was referenced.
@@ -79,67 +87,65 @@ function readPackageSync(_: unknown, file: string): PkgJson {
   return readPackageCached(file);
 }
 
-function createPackageFilter(
-  originalPath: string,
-  userFilter?: ResolverOptions['packageFilter'],
-): ResolverOptions['packageFilter'] {
-  if (shouldIgnoreRequestForExports(originalPath)) {
-    return userFilter;
+function getPathInModule(
+  path: string,
+  options: UpstreamResolveOptionsWithConditions,
+): string {
+  if (shouldIgnoreRequestForExports(path)) {
+    return path;
   }
 
-  return function packageFilter(pkg, ...rest) {
-    let filteredPkg = pkg;
+  const segments = path.split('/');
 
-    if (userFilter) {
-      filteredPkg = userFilter(filteredPkg, ...rest);
-    }
+  let moduleName = segments.shift();
 
-    if (filteredPkg.exports == null) {
-      return filteredPkg;
+  if (moduleName) {
+    // TODO: handle `#` here: https://github.com/facebook/jest/issues/12270
+    if (moduleName.startsWith('@')) {
+      moduleName = `${moduleName}/${segments.shift()}`;
     }
 
-    return {
-      ...filteredPkg,
-      // remove `main` so `resolve` doesn't look at it and confuse the `.`
-      // loading in `pathFilter`
-      main: undefined,
-    };
-  };
-}
+    let packageJsonPath = '';
 
-function createPathFilter(
-  originalPath: string,
-  conditions?: Array<string>,
-  userFilter?: ResolverOptions['pathFilter'],
-): ResolverOptions['pathFilter'] {
-  if (shouldIgnoreRequestForExports(originalPath)) {
-    return userFilter;
-  }
+    try {
+      packageJsonPath = resolveSync(`${moduleName}/package.json`, options);
+    } catch {
+      // ignore if package.json cannot be found
+    }
 
-  const options: ResolveExportsOptions = conditions
-    ? {conditions, unsafe: true}
-    : // no conditions were passed - let's assume this is Jest internal and it should be `require`
-      {browser: false, require: true};
+    if (packageJsonPath && isFile(packageJsonPath)) {
+      const pkg = readPackageCached(packageJsonPath);
 
-  return function pathFilter(pkg, path, relativePath, ...rest) {
-    let pathToUse = relativePath;
+      if (pkg.exports) {
+        // we need to make sure resolve ignores `main`
+        delete pkg.main;
 
-    if (userFilter) {
-      pathToUse = userFilter(pkg, path, relativePath, ...rest);
-    }
+        const subpath = segments.join('/') || '.';
 
-    if (pkg.exports == null) {
-      return pathToUse;
-    }
+        const resolved = resolveExports(
+          pkg,
+          subpath,
+          createResolveOptions(options.conditions),
+        );
 
-    // this `index` thing can backfire, but `resolve` adds it: https://github.com/browserify/resolve/blob/f1b51848ecb7f56f77bfb823511d032489a13eab/lib/sync.js#L192
-    const isRootRequire =
-      pathToUse === 'index' && !originalPath.endsWith('/index');
+        // TODO: should we throw if not?
+        if (resolved) {
+          return pathResolve(dirname(packageJsonPath), resolved);
+        }
+      }
+    }
+  }
 
-    const newPath = isRootRequire ? '.' : slash(pathToUse);
+  return path;
+}
 
-    return resolveExports(pkg, newPath, options) || pathToUse;
-  };
+function createResolveOptions(
+  conditions: Array<string> | undefined,
+): ResolveExportsOptions {
+  return conditions
+    ? {conditions, unsafe: true}
+    : // no conditions were passed - let's assume this is Jest internal and it should be `require`
+      {browser: false, require: true};
 }
 
 // if it's a relative import or an absolute path, exports are ignored
diff --git a/packages/jest-worker/src/__tests__/leak-integration.test.ts b/packages/jest-worker/src/__tests__/leak-integration.test.ts
index 3acfa58be8df..f8e440e2d904 100644
--- a/packages/jest-worker/src/__tests__/leak-integration.test.ts
+++ b/packages/jest-worker/src/__tests__/leak-integration.test.ts
@@ -9,7 +9,7 @@ import {tmpdir} from 'os';
 import {join} from 'path';
 import {writeFileSync} from 'graceful-fs';
 import LeakDetector from 'jest-leak-detector';
-import {Worker} from '../..';
+import {Worker} from '../../build/index';
 
 let workerFile!: string;
 beforeAll(() => {
@@ -30,10 +30,10 @@ afterEach(async () => {
 
 it('does not retain arguments after a task finished', async () => {
   let leakDetector!: LeakDetector;
-  await new Promise(resolve => {
+  await new Promise((resolve, reject) => {
     const obj = {};
     leakDetector = new LeakDetector(obj);
-    (worker as any).fn(obj).then(resolve);
+    (worker as any).fn(obj).then(resolve, reject);
   });
 
   expect(await leakDetector.isLeaking()).toBe(false);