diff --git a/benchmarks/core/parse-headers.mjs b/benchmarks/core/parse-headers.mjs
index 439986da93d..a005b3b33b2 100644
--- a/benchmarks/core/parse-headers.mjs
+++ b/benchmarks/core/parse-headers.mjs
@@ -87,7 +87,7 @@ bench('noop', () => {})
 bench('noop', () => {})
 bench('noop', () => {})
 
-group('parseHeaders', () => {
+group(() => {
   bench('parseHeaders', () => {
     for (let i = 0; i < headers.length; ++i) {
       parseHeaders(headers[i])
diff --git a/lib/core/util.js b/lib/core/util.js
index db8dda53a81..767d586b93a 100644
--- a/lib/core/util.js
+++ b/lib/core/util.js
@@ -440,19 +440,39 @@ function parseHeaders (headers, obj) {
     const key = headerNameToString(headers[i])
     let val = obj[key]
 
-    if (val) {
-      if (typeof val === 'string') {
-        val = [val]
-        obj[key] = val
-      }
-      val.push(headers[i + 1].toString('latin1'))
-    } else {
-      const headersValue = headers[i + 1]
-      if (typeof headersValue === 'string') {
-        obj[key] = headersValue
+    if (val !== undefined) {
+      if (!Object.hasOwn(obj, key)) {
+        const headersValue = typeof headers[i + 1] === 'string'
+          ? headers[i + 1]
+          : Array.isArray(headers[i + 1])
+            ? headers[i + 1].map(x => x.toString('latin1'))
+            : headers[i + 1].toString('latin1')
+
+        if (key === '__proto__') {
+          Object.defineProperty(obj, key, {
+            value: headersValue,
+            enumerable: true,
+            configurable: true,
+            writable: true
+          })
+        } else {
+          obj[key] = headersValue
+        }
       } else {
-        obj[key] = Array.isArray(headersValue) ? headersValue.map(x => x.toString('latin1')) : headersValue.toString('latin1')
+        if (typeof val === 'string') {
+          val = [val]
+          obj[key] = val
+        }
+        val.push(headers[i + 1].toString('latin1'))
       }
+    } else {
+      const headersValue = typeof headers[i + 1] === 'string'
+        ? headers[i + 1]
+        : Array.isArray(headers[i + 1])
+          ? headers[i + 1].map(x => x.toString('latin1'))
+          : headers[i + 1].toString('latin1')
+
+      obj[key] = headersValue
     }
   }
 
diff --git a/test/prototype-headers.js b/test/prototype-headers.js
new file mode 100644
index 00000000000..aa1bf15be26
--- /dev/null
+++ b/test/prototype-headers.js
@@ -0,0 +1,84 @@
+'use strict'
+
+const { test } = require('node:test')
+const assert = require('node:assert')
+const { promisify } = require('node:util')
+const net = require('node:net')
+const { Client } = require('..')
+
+function createRawServer (response) {
+  return net.createServer((socket) => {
+    socket.once('data', () => {
+      socket.end(response)
+    })
+  })
+}
+
+test('request handles response headers that shadow Object.prototype', async (t) => {
+  const server = createRawServer([
+    'HTTP/1.1 200 OK',
+    '__proto__: pwned',
+    'constructor: built-in',
+    'content-length: 2',
+    'connection: close',
+    '',
+    'OK'
+  ].join('\r\n'))
+
+  t.after(() => {
+    server.closeAllConnections?.()
+    server.close()
+  })
+
+  await promisify(server.listen.bind(server))(0)
+
+  const client = new Client(`http://localhost:${server.address().port}`)
+  t.after(() => client.close())
+
+  const { statusCode, headers, body } = await client.request({
+    path: '/',
+    method: 'GET'
+  })
+
+  assert.strictEqual(statusCode, 200)
+  assert.strictEqual(Object.getOwnPropertyDescriptor(headers, '__proto__').value, 'pwned')
+  assert.strictEqual(Object.getOwnPropertyDescriptor(headers, 'constructor').value, 'built-in')
+  assert.strictEqual(await body.text(), 'OK')
+})
+
+test('request handles response trailers that shadow Object.prototype', async (t) => {
+  const server = createRawServer([
+    'HTTP/1.1 200 OK',
+    'transfer-encoding: chunked',
+    'trailer: __proto__, constructor',
+    'connection: close',
+    '',
+    '2',
+    'OK',
+    '0',
+    '__proto__: trailer',
+    'constructor: built-in-trailer',
+    '',
+    ''
+  ].join('\r\n'))
+
+  t.after(() => {
+    server.closeAllConnections?.()
+    server.close()
+  })
+
+  await promisify(server.listen.bind(server))(0)
+
+  const client = new Client(`http://localhost:${server.address().port}`)
+  t.after(() => client.close())
+
+  const { statusCode, trailers, body } = await client.request({
+    path: '/',
+    method: 'GET'
+  })
+
+  assert.strictEqual(statusCode, 200)
+  assert.strictEqual(await body.text(), 'OK')
+  assert.strictEqual(Object.getOwnPropertyDescriptor(trailers, '__proto__').value, 'trailer')
+  assert.strictEqual(Object.getOwnPropertyDescriptor(trailers, 'constructor').value, 'built-in-trailer')
+})