diff --git a/packages/typescript-eslint/package.json b/packages/typescript-eslint/package.json
index f68c8c9991b7..6c0144e06b20 100644
--- a/packages/typescript-eslint/package.json
+++ b/packages/typescript-eslint/package.json
@@ -52,6 +52,7 @@
   "dependencies": {
     "@typescript-eslint/eslint-plugin": "8.36.0",
     "@typescript-eslint/parser": "8.36.0",
+    "@typescript-eslint/typescript-estree": "8.36.0",
     "@typescript-eslint/utils": "8.36.0"
   },
   "peerDependencies": {
diff --git a/packages/typescript-eslint/src/getTSConfigRootDirFromStack.ts b/packages/typescript-eslint/src/getTSConfigRootDirFromStack.ts
new file mode 100644
index 000000000000..01378b1618f3
--- /dev/null
+++ b/packages/typescript-eslint/src/getTSConfigRootDirFromStack.ts
@@ -0,0 +1,16 @@
+import { fileURLToPath } from 'node:url';
+
+export function getTSConfigRootDirFromStack(stack: string): string | undefined {
+  for (const line of stack.split('\n').map(line => line.trim())) {
+    const candidate = /(\S+)eslint\.config\.(c|m)?(j|t)s/.exec(line)?.[1];
+    if (!candidate) {
+      continue;
+    }
+
+    return candidate.startsWith('file://')
+      ? fileURLToPath(candidate)
+      : candidate;
+  }
+
+  return undefined;
+}
diff --git a/packages/typescript-eslint/src/index.ts b/packages/typescript-eslint/src/index.ts
index 86870c855cd0..9892ede6065a 100644
--- a/packages/typescript-eslint/src/index.ts
+++ b/packages/typescript-eslint/src/index.ts
@@ -3,8 +3,10 @@ import type { TSESLint } from '@typescript-eslint/utils';
 
 import pluginBase from '@typescript-eslint/eslint-plugin';
 import rawPlugin from '@typescript-eslint/eslint-plugin/use-at-your-own-risk/raw-plugin';
+import { addCandidateTSConfigRootDir } from '@typescript-eslint/typescript-estree';
 
 import { config } from './config-helper';
+import { getTSConfigRootDirFromStack } from './getTSConfigRootDirFromStack';
 
 export const parser: TSESLint.FlatConfig.Parser = rawPlugin.parser;
 
@@ -36,7 +38,7 @@ export const plugin: TSESLint.FlatConfig.Plugin = pluginBase as Omit<
   'configs'
 >;
 
-export const configs = {
+export const configs = createConfigsGetters({
   /**
    * Enables each the rules provided as a part of typescript-eslint. Note that many rules are not applicable in all codebases, or are meant to be configured.
    * @see {@link https://typescript-eslint.io/users/configs#all}
@@ -120,7 +122,36 @@ export const configs = {
    */
   stylisticTypeCheckedOnly:
     rawPlugin.flatConfigs['flat/stylistic-type-checked-only'],
-};
+});
+
+function createConfigsGetters<T extends object>(values: T): T {
+  const configs = {};
+
+  Object.defineProperties(
+    configs,
+    Object.fromEntries(
+      Object.entries(values).map(([key, value]: [string, unknown]) => [
+        key,
+        {
+          enumerable: true,
+          get: () => {
+            const candidateRootDir = getTSConfigRootDirFromStack(
+              // eslint-disable-next-line @typescript-eslint/no-non-null-assertion
+              new Error().stack!,
+            );
+            if (candidateRootDir) {
+              addCandidateTSConfigRootDir(candidateRootDir);
+            }
+
+            return value;
+          },
+        },
+      ]),
+    ),
+  );
+
+  return configs as T;
+}
 
 export type Config = TSESLint.FlatConfig.ConfigFile;
 
diff --git a/packages/typescript-eslint/tests/configs.test.ts b/packages/typescript-eslint/tests/configs.test.ts
index fea7a41196f4..cac7e4f46bd6 100644
--- a/packages/typescript-eslint/tests/configs.test.ts
+++ b/packages/typescript-eslint/tests/configs.test.ts
@@ -4,9 +4,25 @@ import type {
 } from '@typescript-eslint/utils/ts-eslint';
 
 import rules from '@typescript-eslint/eslint-plugin/use-at-your-own-risk/rules';
+import { clearCandidateTSConfigRootDirs } from '@typescript-eslint/typescript-estree';
 
 import tseslint from '../src/index.js';
 
+vi.mock('@typescript-eslint/typescript-estree', async () => ({
+  ...(await vi.importActual('@typescript-eslint/typescript-estree')),
+  get addCandidateTSConfigRootDir() {
+    return mockAddCandidateTSConfigRootDir;
+  },
+}));
+
+const mockGetTSConfigRootDirFromStack = vi.fn();
+
+vi.mock('../src/getTSConfigRootDirFromStack', () => ({
+  get getTSConfigRootDirFromStack() {
+    return mockGetTSConfigRootDirFromStack;
+  },
+}));
+
 const RULE_NAME_PREFIX = '@typescript-eslint/';
 const EXTENSION_RULES = Object.entries(rules)
   .filter(([, rule]) => rule.meta.docs.extendsBaseRule)
@@ -384,3 +400,36 @@ describe('stylistic-type-checked-only.ts', () => {
     },
   );
 });
+
+const mockAddCandidateTSConfigRootDir = vi.fn();
+
+describe('Candidate tsconfigRootDirs', () => {
+  beforeEach(() => {
+    clearCandidateTSConfigRootDirs();
+    mockAddCandidateTSConfigRootDir.mockClear();
+  });
+
+  describe.each(Object.keys(tseslint.configs))('%s', configKey => {
+    it('does not populate a candidate tsconfigRootDir when accessed and one cannot be inferred from the stack', () => {
+      mockGetTSConfigRootDirFromStack.mockReturnValue(undefined);
+
+      // eslint-disable-next-line @typescript-eslint/no-unused-expressions
+      tseslint.configs[configKey as keyof typeof tseslint.configs];
+
+      expect(mockAddCandidateTSConfigRootDir).not.toHaveBeenCalled();
+    });
+
+    it('populates a candidate tsconfigRootDir when accessed and one can be inferred from the stack', () => {
+      const tsconfigRootDir = 'a/b/c/';
+
+      mockGetTSConfigRootDirFromStack.mockReturnValue(tsconfigRootDir);
+
+      // eslint-disable-next-line @typescript-eslint/no-unused-expressions
+      tseslint.configs[configKey as keyof typeof tseslint.configs];
+
+      expect(mockAddCandidateTSConfigRootDir).toHaveBeenCalledWith(
+        tsconfigRootDir,
+      );
+    });
+  });
+});
diff --git a/packages/typescript-eslint/tests/getTsconfigRootDirFromStack.test.ts b/packages/typescript-eslint/tests/getTsconfigRootDirFromStack.test.ts
new file mode 100644
index 000000000000..57a3b0b5f2a3
--- /dev/null
+++ b/packages/typescript-eslint/tests/getTsconfigRootDirFromStack.test.ts
@@ -0,0 +1,54 @@
+import path from 'node:path';
+
+import { getTSConfigRootDirFromStack } from '../src/getTSConfigRootDirFromStack';
+
+const isWindows = process.platform === 'win32';
+
+describe(getTSConfigRootDirFromStack, () => {
+  it('returns undefined when no file path seems to be an ESLint config', () => {
+    const actual = getTSConfigRootDirFromStack(
+      [
+        `Error`,
+        ' at file:///other.config.js',
+        ' at ModuleJob.run',
+        'at async NodeHfs.walk(...)',
+      ].join('\n'),
+    );
+
+    expect(actual).toBeUndefined();
+  });
+
+  it.runIf(!isWindows)(
+    'returns a Posix config file path when a file:// path to an ESLint config is in the stack',
+    () => {
+      const actual = getTSConfigRootDirFromStack(
+        [
+          `Error`,
+          ' at file:///path/to/file/eslint.config.js',
+          ' at ModuleJob.run',
+          'at async NodeHfs.walk(...)',
+        ].join('\n'),
+      );
+
+      expect(actual).toBe('/path/to/file/');
+    },
+  );
+
+  it.each(['cjs', 'cts', 'js', 'mjs', 'mts', 'ts'])(
+    'returns the path to the config file when its extension is %s',
+    extension => {
+      const expected = isWindows ? 'C:\\path\\to\\file\\' : '/path/to/file/';
+
+      const actual = getTSConfigRootDirFromStack(
+        [
+          `Error`,
+          ` at ${path.join(expected, `eslint.config.${extension}`)}`,
+          ' at ModuleJob.run',
+          'at async NodeHfs.walk(...)',
+        ].join('\n'),
+      );
+
+      expect(actual).toBe(expected);
+    },
+  );
+});
diff --git a/packages/typescript-eslint/tsconfig.build.json b/packages/typescript-eslint/tsconfig.build.json
index c41d1d4c30ed..8f377becd3cd 100644
--- a/packages/typescript-eslint/tsconfig.build.json
+++ b/packages/typescript-eslint/tsconfig.build.json
@@ -2,6 +2,9 @@
   "extends": "../../tsconfig.build.json",
   "compilerOptions": {},
   "references": [
+    {
+      "path": "../typescript-estree/tsconfig.build.json"
+    },
     {
       "path": "../utils/tsconfig.build.json"
     },
diff --git a/packages/typescript-eslint/tsconfig.json b/packages/typescript-eslint/tsconfig.json
index d12794a533bf..f94f467e0b00 100644
--- a/packages/typescript-eslint/tsconfig.json
+++ b/packages/typescript-eslint/tsconfig.json
@@ -3,6 +3,9 @@
   "files": [],
   "include": [],
   "references": [
+    {
+      "path": "../typescript-estree"
+    },
     {
       "path": "../utils"
     },
diff --git a/packages/typescript-estree/src/clear-caches.ts b/packages/typescript-estree/src/clear-caches.ts
index 5e9867d3beab..3d5897953b70 100644
--- a/packages/typescript-estree/src/clear-caches.ts
+++ b/packages/typescript-estree/src/clear-caches.ts
@@ -3,6 +3,7 @@ import {
   clearDefaultProjectMatchedFiles,
   clearProgramCache as clearProgramCacheOriginal,
 } from './parser';
+import { clearCandidateTSConfigRootDirs } from './parseSettings/candidateTSConfigRootDirs';
 import {
   clearTSConfigMatchCache,
   clearTSServerProjectService,
@@ -17,6 +18,7 @@ import { clearGlobCache } from './parseSettings/resolveProjectList';
  * - In custom lint tooling that iteratively lints one project at a time to prevent OOMs.
  */
 export function clearCaches(): void {
+  clearCandidateTSConfigRootDirs();
   clearDefaultProjectMatchedFiles();
   clearProgramCacheOriginal();
   clearWatchCaches();
diff --git a/packages/typescript-estree/src/index.ts b/packages/typescript-estree/src/index.ts
index 39e921e8762a..654ea73982d2 100644
--- a/packages/typescript-estree/src/index.ts
+++ b/packages/typescript-estree/src/index.ts
@@ -16,6 +16,10 @@ export type {
   ParserServicesWithTypeInformation,
   TSESTreeOptions,
 } from './parser-options';
+export {
+  addCandidateTSConfigRootDir,
+  clearCandidateTSConfigRootDirs,
+} from './parseSettings/candidateTSConfigRootDirs';
 export { simpleTraverse } from './simple-traverse';
 export * from './ts-estree';
 export { typescriptVersionIsAtLeast } from './version-check';
diff --git a/packages/typescript-estree/src/parseSettings/candidateTSConfigRootDirs.ts b/packages/typescript-estree/src/parseSettings/candidateTSConfigRootDirs.ts
new file mode 100644
index 000000000000..13e19c8aac8a
--- /dev/null
+++ b/packages/typescript-estree/src/parseSettings/candidateTSConfigRootDirs.ts
@@ -0,0 +1,31 @@
+const candidateTSConfigRootDirs = new Set<string>();
+
+export function addCandidateTSConfigRootDir(candidate: string): void {
+  candidateTSConfigRootDirs.add(candidate);
+}
+
+export function clearCandidateTSConfigRootDirs(): void {
+  candidateTSConfigRootDirs.clear();
+}
+
+export function getInferredTSConfigRootDir(): string {
+  const entries = [...candidateTSConfigRootDirs];
+
+  switch (entries.length) {
+    case 0:
+      return process.cwd();
+
+    case 1:
+      return entries[0];
+
+    default:
+      throw new Error(
+        [
+          'No tsconfigRootDir was set, and multiple candidate TSConfigRootDirs are present:',
+          ...entries.map(candidate => ` - ${candidate}`),
+          "You'll need to explicitly set tsconfigRootDir in your parser options.",
+          'See: https://typescript-eslint.io/packages/parser/#tsconfigrootdir',
+        ].join('\n'),
+      );
+  }
+}
diff --git a/packages/typescript-estree/src/parseSettings/createParseSettings.ts b/packages/typescript-estree/src/parseSettings/createParseSettings.ts
index 678b771ac3a5..6710e36b870f 100644
--- a/packages/typescript-estree/src/parseSettings/createParseSettings.ts
+++ b/packages/typescript-estree/src/parseSettings/createParseSettings.ts
@@ -15,6 +15,7 @@ import type { MutableParseSettings } from './index';
 import { ensureAbsolutePath } from '../create-program/shared';
 import { validateDefaultProjectForFilesGlob } from '../create-program/validateDefaultProjectForFilesGlob';
 import { isSourceFile } from '../source-files';
+import { getInferredTSConfigRootDir } from './candidateTSConfigRootDirs';
 import {
   DEFAULT_TSCONFIG_CACHE_DURATION_SECONDS,
   ExpiringCache,
@@ -52,7 +53,7 @@ export function createParseSettings(
   const tsconfigRootDir =
     typeof tsestreeOptions.tsconfigRootDir === 'string'
       ? tsestreeOptions.tsconfigRootDir
-      : process.cwd();
+      : getInferredTSConfigRootDir();
   const passedLoggerFn = typeof tsestreeOptions.loggerFn === 'function';
   const filePath = ensureAbsolutePath(
     typeof tsestreeOptions.filePath === 'string' &&
diff --git a/packages/typescript-estree/tests/lib/candidateTSConfigRootDirs.test.ts b/packages/typescript-estree/tests/lib/candidateTSConfigRootDirs.test.ts
new file mode 100644
index 000000000000..7536d56a205d
--- /dev/null
+++ b/packages/typescript-estree/tests/lib/candidateTSConfigRootDirs.test.ts
@@ -0,0 +1,40 @@
+import { addCandidateTSConfigRootDir } from '../../src';
+import {
+  clearCandidateTSConfigRootDirs,
+  getInferredTSConfigRootDir,
+} from '../../src/parseSettings/candidateTSConfigRootDirs';
+
+describe(getInferredTSConfigRootDir, () => {
+  beforeEach(() => {
+    clearCandidateTSConfigRootDirs();
+  });
+
+  it('returns process.cwd() when there are no candidates', () => {
+    const actual = getInferredTSConfigRootDir();
+
+    expect(actual).toBe(process.cwd());
+  });
+
+  it('returns the candidate when there is one candidate', () => {
+    const candidate = 'a/b/c';
+    addCandidateTSConfigRootDir(candidate);
+
+    const actual = getInferredTSConfigRootDir();
+
+    expect(actual).toBe(candidate);
+  });
+
+  it('throws an error when there are multiple candidates', () => {
+    addCandidateTSConfigRootDir('a');
+    addCandidateTSConfigRootDir('b');
+
+    expect(() => getInferredTSConfigRootDir())
+      .toThrowErrorMatchingInlineSnapshot(`
+        [Error: No tsconfigRootDir was set, and multiple candidate TSConfigRootDirs are present:
+         - a
+         - b
+        You'll need to explicitly set tsconfigRootDir in your parser options.
+        See: https://typescript-eslint.io/packages/parser/#tsconfigrootdir]
+      `);
+  });
+});
diff --git a/packages/typescript-estree/tests/lib/createParseSettings.test.ts b/packages/typescript-estree/tests/lib/createParseSettings.test.ts
index ccb210fd8dbd..d3f5fea99819 100644
--- a/packages/typescript-estree/tests/lib/createParseSettings.test.ts
+++ b/packages/typescript-estree/tests/lib/createParseSettings.test.ts
@@ -1,3 +1,7 @@
+import {
+  addCandidateTSConfigRootDir,
+  clearCandidateTSConfigRootDirs,
+} from '../../src/parseSettings/candidateTSConfigRootDirs';
 import { createParseSettings } from '../../src/parseSettings/createParseSettings';
 
 const projectService = { service: true };
@@ -61,4 +65,36 @@ describe(createParseSettings, () => {
       );
     });
   });
+
+  describe('tsconfigRootDir', () => {
+    beforeEach(() => {
+      clearCandidateTSConfigRootDirs();
+    });
+
+    it('uses the provided tsconfigRootDir when it exists and no candidates exist', () => {
+      const tsconfigRootDir = 'a/b/c';
+
+      const parseSettings = createParseSettings('', { tsconfigRootDir });
+
+      expect(parseSettings.tsconfigRootDir).toBe(tsconfigRootDir);
+    });
+
+    it('uses the provided tsconfigRootDir when it exists and a candidate exists', () => {
+      addCandidateTSConfigRootDir('candidate');
+      const tsconfigRootDir = 'a/b/c';
+
+      const parseSettings = createParseSettings('', { tsconfigRootDir });
+
+      expect(parseSettings.tsconfigRootDir).toBe(tsconfigRootDir);
+    });
+
+    it('uses the inferred candidate when no tsconfigRootDir is provided and a candidate exists', () => {
+      const tsconfigRootDir = 'a/b/c';
+      addCandidateTSConfigRootDir(tsconfigRootDir);
+
+      const parseSettings = createParseSettings('');
+
+      expect(parseSettings.tsconfigRootDir).toBe(tsconfigRootDir);
+    });
+  });
 });
diff --git a/yarn.lock b/yarn.lock
index a4ac6c4b95ec..08bde6338a88 100644
--- a/yarn.lock
+++ b/yarn.lock
@@ -19802,6 +19802,7 @@ __metadata:
   dependencies:
     "@typescript-eslint/eslint-plugin": 8.36.0
     "@typescript-eslint/parser": 8.36.0
+    "@typescript-eslint/typescript-estree": 8.36.0
     "@typescript-eslint/utils": 8.36.0
     "@vitest/coverage-v8": ^3.1.3
     eslint: "*"

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