diff --git a/src/events/http/lambda-events/LambdaProxyIntegrationEventV2.js b/src/events/http/lambda-events/LambdaProxyIntegrationEventV2.js
index a506951a5..70bdf5630 100644
--- a/src/events/http/lambda-events/LambdaProxyIntegrationEventV2.js
+++ b/src/events/http/lambda-events/LambdaProxyIntegrationEventV2.js
@@ -5,6 +5,7 @@ import {
   formatToClfTime,
   nullIfEmpty,
   parseHeaders,
+  lowerCaseKeys,
 } from '../../../utils/index.js'
 
 const { isArray } = Array
@@ -71,7 +72,7 @@ export default class LambdaProxyIntegrationEventV2 {
     const { rawHeaders } = this.#request.raw.req
 
     // NOTE FIXME request.raw.req.rawHeaders can only be null for testing (hapi shot inject())
-    const headers = parseHeaders(rawHeaders || []) || {}
+    const headers = lowerCaseKeys(parseHeaders(rawHeaders || [])) || {}
 
     if (headers['sls-offline-authorizer-override']) {
       try {
@@ -96,23 +97,17 @@ export default class LambdaProxyIntegrationEventV2 {
       }
 
       if (
-        !headers['Content-Length'] &&
         !headers['content-length'] &&
-        !headers['Content-length'] &&
         (typeof body === 'string' ||
           body instanceof Buffer ||
           body instanceof ArrayBuffer)
       ) {
-        headers['Content-Length'] = String(Buffer.byteLength(body))
+        headers['content-length'] = String(Buffer.byteLength(body))
       }
 
       // Set a default Content-Type if not provided.
-      if (
-        !headers['Content-Type'] &&
-        !headers['content-type'] &&
-        !headers['Content-type']
-      ) {
-        headers['Content-Type'] = 'application/json'
+      if (!headers['content-type']) {
+        headers['content-type'] = 'application/json'
       }
     } else if (typeof body === 'undefined' || body === '') {
       body = null
diff --git a/src/utils/__tests__/lowerCaseKeys.test.js b/src/utils/__tests__/lowerCaseKeys.test.js
new file mode 100644
index 000000000..682da3795
--- /dev/null
+++ b/src/utils/__tests__/lowerCaseKeys.test.js
@@ -0,0 +1,28 @@
+import lowerCaseKeys from '../lowerCaseKeys.js'
+
+describe('lowerCaseKeys', () => {
+  test(`should handle empty object`, () => {
+    const result = lowerCaseKeys({})
+    expect(result).toEqual({})
+  })
+
+  test(`should handle object with one key`, () => {
+    const result = lowerCaseKeys({ 'Some-Key': 'value' })
+    expect(result).toEqual({ 'some-key': 'value' })
+  })
+
+  test(`should handle object with multiple keys`, () => {
+    const result = lowerCaseKeys({
+      'Some-Key': 'value',
+      'Another-Key': 'anotherValue',
+      'lOts-OF-CAPitaLs': 'ButThisIsNotTouched',
+      'already-lowercase': 'cool',
+    })
+    expect(result).toEqual({
+      'some-key': 'value',
+      'another-key': 'anotherValue',
+      'lots-of-capitals': 'ButThisIsNotTouched',
+      'already-lowercase': 'cool',
+    })
+  })
+})
diff --git a/src/utils/index.js b/src/utils/index.js
index bdaa721eb..c70d418a6 100644
--- a/src/utils/index.js
+++ b/src/utils/index.js
@@ -4,6 +4,7 @@ export { default as detectExecutable } from './detectExecutable.js'
 export { default as formatToClfTime } from './formatToClfTime.js'
 export { default as getHttpApiCorsConfig } from './getHttpApiCorsConfig.js'
 export { default as jsonPath } from './jsonPath.js'
+export { default as lowerCaseKeys } from './lowerCaseKeys.js'
 export { default as parseHeaders } from './parseHeaders.js'
 export { default as parseMultiValueHeaders } from './parseMultiValueHeaders.js'
 export { default as parseMultiValueQueryStringParameters } from './parseMultiValueQueryStringParameters.js'
diff --git a/src/utils/lowerCaseKeys.js b/src/utils/lowerCaseKeys.js
new file mode 100644
index 000000000..b6480ee5a
--- /dev/null
+++ b/src/utils/lowerCaseKeys.js
@@ -0,0 +1,6 @@
+const { entries, fromEntries } = Object
+
+// (obj: { [string]: string }): { [Lowercase<string>]: string }
+export default function parseHeaders(obj) {
+  return fromEntries(entries(obj).map(([k, v]) => [k.toLowerCase(), v]))
+}
diff --git a/tests/integration/httpApi-headers/handler.js b/tests/integration/httpApi-headers/handler.js
new file mode 100644
index 000000000..b801a5864
--- /dev/null
+++ b/tests/integration/httpApi-headers/handler.js
@@ -0,0 +1,10 @@
+'use strict'
+
+exports.echoHeaders = async function get(event) {
+  return {
+    body: JSON.stringify({
+      headersReceived: event.headers,
+    }),
+    statusCode: 200,
+  }
+}
diff --git a/tests/integration/httpApi-headers/httpApi-headers.test.js b/tests/integration/httpApi-headers/httpApi-headers.test.js
new file mode 100644
index 000000000..ac787ca91
--- /dev/null
+++ b/tests/integration/httpApi-headers/httpApi-headers.test.js
@@ -0,0 +1,38 @@
+import { resolve } from 'path'
+import fetch from 'node-fetch'
+import { joinUrl, setup, teardown } from '../_testHelpers/index.js'
+
+jest.setTimeout(30000)
+
+describe('HttpApi Headers Tests', () => {
+  // init
+  beforeAll(() =>
+    setup({
+      servicePath: resolve(__dirname),
+    }),
+  )
+
+  // cleanup
+  afterAll(() => teardown())
+
+  test.each(['GET', 'POST'])('%s headers', async (method) => {
+    const url = joinUrl(TEST_BASE_URL, '/echo-headers')
+    const options = {
+      method,
+      headers: {
+        Origin: 'http://www.example.com',
+        'X-Webhook-Signature': 'ABCDEF',
+      },
+    }
+
+    const response = await fetch(url, options)
+    expect(response.status).toEqual(200)
+
+    const body = await response.json()
+
+    expect(body.headersReceived).toMatchObject({
+      origin: 'http://www.example.com',
+      'x-webhook-signature': 'ABCDEF',
+    })
+  })
+})
diff --git a/tests/integration/httpApi-headers/serverless.yml b/tests/integration/httpApi-headers/serverless.yml
new file mode 100644
index 000000000..23fd19afe
--- /dev/null
+++ b/tests/integration/httpApi-headers/serverless.yml
@@ -0,0 +1,25 @@
+service: httpapi-headers
+
+plugins:
+  - ../../../
+
+provider:
+  memorySize: 128
+  name: aws
+  region: us-east-1 # default
+  runtime: nodejs12.x
+  stage: dev
+  versionFunctions: false
+  httpApi:
+    payload: '2.0'
+
+functions:
+  echoHeaders:
+    events:
+      - httpApi:
+          method: get
+          path: echo-headers
+      - httpApi:
+          method: post
+          path: echo-headers
+    handler: handler.echoHeaders