diff --git a/src/exportMap/childContext.js b/src/exportMap/childContext.js
index 3534c5913..cf8135f12 100644
--- a/src/exportMap/childContext.js
+++ b/src/exportMap/childContext.js
@@ -1,7 +1,7 @@
 import { hashObject } from 'eslint-module-utils/hash';
 
-let parserOptionsHash = '';
-let prevParserOptions = '';
+let optionsHash = '';
+let prevOptions = '';
 let settingsHash = '';
 let prevSettings = '';
 
@@ -17,13 +17,35 @@ export default function childContext(path, context) {
     prevSettings = JSON.stringify(settings);
   }
 
-  if (JSON.stringify(parserOptions) !== prevParserOptions) {
-    parserOptionsHash = hashObject({ parserOptions }).digest('hex');
-    prevParserOptions = JSON.stringify(parserOptions);
+  // We'll use either a combination of `parserOptions` and `parserPath` or `languageOptions`
+  // to construct the cache key, depending on whether this is using a flat config or not.
+  let optionsToken;
+  if (!parserPath && languageOptions) {
+    // Replacer function helps us with serializing the parser nested within `languageOptions`.
+    const replacerFn = (_, value) => {
+      if (typeof value === 'function') {
+        return value.toString();
+      }
+      return value;
+    };
+    if (JSON.stringify(languageOptions, replacerFn) !== prevOptions) {
+      optionsHash = hashObject({ languageOptions }).digest('hex');
+      prevOptions = JSON.stringify(languageOptions, replacerFn);
+    }
+    // For languageOptions, we're just using the hashed options as the options token
+    optionsToken = optionsHash;
+  } else {
+    if (JSON.stringify(parserOptions) !== prevOptions) {
+      optionsHash = hashObject({ parserOptions }).digest('hex');
+      prevOptions = JSON.stringify(parserOptions);
+    }
+    // When not using flat config, we use a combination of the hashed parserOptions
+    // and parserPath as the token
+    optionsToken = String(parserPath) + optionsHash;
   }
 
   return {
-    cacheKey: String(parserPath) + parserOptionsHash + settingsHash + String(path),
+    cacheKey: optionsToken + settingsHash + String(path),
     settings,
     parserOptions,
     parserPath,
diff --git a/tests/src/exportMap/childContext.js b/tests/src/exportMap/childContext.js
index 06fa04afe..16652f9dc 100644
--- a/tests/src/exportMap/childContext.js
+++ b/tests/src/exportMap/childContext.js
@@ -1,4 +1,5 @@
 import { expect } from 'chai';
+import { hashObject } from 'eslint-module-utils/hash';
 
 import childContext from '../../../src/exportMap/childContext';
 
@@ -16,8 +17,13 @@ describe('childContext', () => {
   const languageOptions = {
     ecmaVersion: 2024,
     sourceType: 'module',
-    parser: {},
+    parser: {
+      parseForESLint() {},
+    },
   };
+  const languageOptionsHash = hashObject({ languageOptions }).digest('hex');
+  const parserOptionsHash = hashObject({ parserOptions }).digest('hex');
+  const settingsHash = hashObject({ settings }).digest('hex');
 
   // https://github.com/import-js/eslint-plugin-import/issues/3051
   it('should pass context properties through, if present', () => {
@@ -48,4 +54,69 @@ describe('childContext', () => {
     expect(result.path).to.equal(path);
     expect(result.cacheKey).to.be.a('string');
   });
+
+  it('should construct cache key out of languageOptions if present', () => {
+    const mockContext = {
+      settings,
+      languageOptions,
+    };
+
+    const result = childContext(path, mockContext);
+
+    expect(result.cacheKey).to.equal(languageOptionsHash + settingsHash + path);
+  });
+
+  it('should use the same cache key upon multiple calls', () => {
+    const mockContext = {
+      settings,
+      languageOptions,
+    };
+
+    let result = childContext(path, mockContext);
+
+    const expectedCacheKey = languageOptionsHash + settingsHash + path;
+    expect(result.cacheKey).to.equal(expectedCacheKey);
+
+    result = childContext(path, mockContext);
+    expect(result.cacheKey).to.equal(expectedCacheKey);
+  });
+
+  it('should update cacheKey if different languageOptions are passed in', () => {
+    const mockContext = {
+      settings,
+      languageOptions,
+    };
+
+    let result = childContext(path, mockContext);
+
+    const firstCacheKey = languageOptionsHash + settingsHash + path;
+    expect(result.cacheKey).to.equal(firstCacheKey);
+
+    // Second run with different parser
+    mockContext.languageOptions = {
+      ...languageOptions,
+      parser: {
+        parseForESLint() {},
+        parse() {},
+      },
+    };
+
+    result = childContext(path, mockContext);
+
+    const secondCacheKey = hashObject({ languageOptions: mockContext.languageOptions }).digest('hex') + settingsHash + path;
+    expect(result.cacheKey).to.not.equal(firstCacheKey);
+    expect(result.cacheKey).to.equal(secondCacheKey);
+  });
+
+  it('should construct cache key out of parserOptions and parserPath if no languageOptions', () => {
+    const mockContext = {
+      settings,
+      parserOptions,
+      parserPath,
+    };
+
+    const result = childContext(path, mockContext);
+
+    expect(result.cacheKey).to.equal(String(parserPath) + parserOptionsHash + settingsHash + path);
+  });
 });