diff --git a/packages/typescript-eslint/src/getTSConfigRootDirFromStack.ts b/packages/typescript-eslint/src/getTSConfigRootDirFromStack.ts
index 01378b1618f..738e016496d 100644
--- a/packages/typescript-eslint/src/getTSConfigRootDirFromStack.ts
+++ b/packages/typescript-eslint/src/getTSConfigRootDirFromStack.ts
@@ -2,7 +2,10 @@ 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];
+    const candidate = /(.+?)[/\\]+eslint\.config\.(c|m)?(j|t)s/
+      .exec(line)?.[1]
+      ?.replace(/\s*at\s+(async\s+)?/g, '')
+      .replaceAll(/^\S+\s+\(/g, '');
     if (!candidate) {
       continue;
     }
diff --git a/packages/typescript-eslint/tests/getTsconfigRootDirFromStack.test.ts b/packages/typescript-eslint/tests/getTsconfigRootDirFromStack.test.ts
index 57a3b0b5f2a..fcc66a041c8 100644
--- a/packages/typescript-eslint/tests/getTsconfigRootDirFromStack.test.ts
+++ b/packages/typescript-eslint/tests/getTsconfigRootDirFromStack.test.ts
@@ -24,20 +24,20 @@ describe(getTSConfigRootDirFromStack, () => {
       const actual = getTSConfigRootDirFromStack(
         [
           `Error`,
-          ' at file:///path/to/file/eslint.config.js',
+          ' at file:///path/to/dir/eslint.config.js',
           ' at ModuleJob.run',
           'at async NodeHfs.walk(...)',
         ].join('\n'),
       );
 
-      expect(actual).toBe('/path/to/file/');
+      expect(actual).toBe('/path/to/dir');
     },
   );
 
   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 expected = isWindows ? 'C:\\path\\to\\dir' : '/path/to/dir';
 
       const actual = getTSConfigRootDirFromStack(
         [
@@ -51,4 +51,83 @@ describe(getTSConfigRootDirFromStack, () => {
       expect(actual).toBe(expected);
     },
   );
+
+  it('returns the full path when it contains a space', () => {
+    const actual = getTSConfigRootDirFromStack(
+      [
+        `Error`,
+        ` at /path/with space/to/dir/eslint.config.ts`,
+        ' at ModuleJob.run',
+      ].join('\n'),
+    );
+
+    expect(actual).toBe('/path/with space/to/dir');
+  });
+
+  it('returns the full path when it contains a space after an async import', () => {
+    const actual = getTSConfigRootDirFromStack(
+      [
+        `Error`,
+        ` at async /path/with space/to/dir/eslint.config.ts`,
+        ' at ModuleJob.run',
+      ].join('\n'),
+    );
+
+    expect(actual).toBe('/path/with space/to/dir');
+  });
+
+  it('returns the full path when it contains multiple spaces', () => {
+    const actual = getTSConfigRootDirFromStack(
+      [
+        `Error`,
+        ` at /path/with spaces to dir/eslint.config.ts`,
+        ' at ModuleJob.run',
+      ].join('\n'),
+    );
+
+    expect(actual).toBe('/path/with spaces to dir');
+  });
+
+  it('returns just the path when prefixed with getter information', () => {
+    const actual = getTSConfigRootDirFromStack(
+      [
+        'Error',
+        'at Object.<anonymous> (/Users/myusername/src/repros/Has Space/eslint.config.js:4:13)',
+        'at Module._compile (node:internal/modules/cjs/loader:1692:14)',
+      ].join('\n'),
+    );
+
+    expect(actual).toBe('/Users/myusername/src/repros/Has Space');
+  });
+
+  it("doesn't get tricked by a not-an-eslint.config.js", () => {
+    const actual = getTSConfigRootDirFromStack(
+      [
+        `Error`,
+        ' at file:///a/b/not-an-eslint.config.js',
+        ' at ModuleJob.run',
+        'at async NodeHfs.walk(...)',
+      ].join('\n'),
+    );
+
+    expect(actual).toBeUndefined();
+  });
+
+  it.each(['cjs', 'cts', 'js', 'mjs', 'mts', 'ts'])(
+    'correctly resolves the config file even when multiple path seps are present %s',
+    extension => {
+      const expected = isWindows ? 'C:\\path\\to\\dir' : '/path/to/dir';
+
+      const actual = getTSConfigRootDirFromStack(
+        [
+          `Error`,
+          ` at ${expected + path.sep + path.sep}eslint.config.${extension}}`,
+          ' at ModuleJob.run',
+          'at async NodeHfs.walk(...)',
+        ].join('\n'),
+      );
+
+      expect(actual).toBe(expected);
+    },
+  );
 });

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