diff --git a/lib/core/util.js b/lib/core/util.js
index f00ddfce0d1..6d0409f87c8 100644
--- a/lib/core/util.js
+++ b/lib/core/util.js
@@ -417,6 +417,30 @@ function bufferToLowerCasedHeaderName (value) {
   return tree.lookup(value) ?? value.toString('latin1').toLowerCase()
 }
 
+/**
+ * Writes a header onto a plain object without going through the
+ * `Object.prototype` `__proto__` setter. Plain assignment there drops a string
+ * value and, when the value is an array, replaces the object's prototype
+ * instead of storing anything. Every other name is a normal assignment.
+ *
+ * @param {Record<string, string | string[]>} obj Accumulator to write onto
+ * @param {string} key Header name
+ * @param {string | string[]} value Header value
+ * @returns {void}
+ */
+function setHeader (obj, key, value) {
+  if (key === '__proto__') {
+    Object.defineProperty(obj, key, {
+      value,
+      enumerable: true,
+      configurable: true,
+      writable: true
+    })
+  } else {
+    obj[key] = value
+  }
+}
+
 /**
  * @param {(Buffer | string)[]} headers
  * @param {Record<string, string | string[]>} [obj]
@@ -1022,6 +1046,7 @@ module.exports = {
   toRawHeaders,
   encodeRawHeaders,
   parseHeaders,
+  setHeader,
   parseKeepAliveTimeout,
   destroy,
   bodyLength,
diff --git a/lib/dispatcher/client-h2.js b/lib/dispatcher/client-h2.js
index bc401008f00..564c33a842d 100644
--- a/lib/dispatcher/client-h2.js
+++ b/lib/dispatcher/client-h2.js
@@ -830,25 +830,27 @@ function buildRequestHeaders (reqHeaders) {
   for (let n = 0; n < reqHeaders.length; n += 2) {
     const key = reqHeaders[n + 0]
     const val = reqHeaders[n + 1]
-    const current = headers[key]
+    // Reading headers[key] directly resolves `__proto__` through the prototype
+    // chain instead of reporting the header as absent.
+    const current = Object.hasOwn(headers, key) ? headers[key] : undefined
 
     if (key === 'cookie') {
       if (current != null) {
-        headers[key] = Array.isArray(current) ? (current.push(val), current) : [current, val]
+        util.setHeader(headers, key, Array.isArray(current) ? (current.push(val), current) : [current, val])
       } else {
-        headers[key] = val
+        util.setHeader(headers, key, val)
       }
 
       continue
     }
 
     if (typeof val === 'string') {
-      headers[key] = current ? `${current}, ${val}` : val
+      util.setHeader(headers, key, current ? `${current}, ${val}` : val)
       continue
     }
 
     for (let i = 0; i < val.length; i++) {
-      headers[key] = headers[key] ? `${headers[key]}, ${val[i]}` : val[i]
+      util.setHeader(headers, key, Object.hasOwn(headers, key) ? `${headers[key]}, ${val[i]}` : val[i])
     }
   }
 
diff --git a/lib/mock/snapshot-recorder.js b/lib/mock/snapshot-recorder.js
index 57a7e7a41dd..e69bcc5a777 100644
--- a/lib/mock/snapshot-recorder.js
+++ b/lib/mock/snapshot-recorder.js
@@ -4,6 +4,7 @@ const { writeFile, readFile, mkdir } = require('node:fs/promises')
 const { dirname, resolve } = require('node:path')
 const { setTimeout, clearTimeout } = require('node:timers')
 const { InvalidArgumentError, UndiciError } = require('../core/errors')
+const { setHeader } = require('../core/util')
 const { hashId, isUrlExcludedFactory, normalizeHeaders, createHeaderFilters } = require('./snapshot-utils')
 
 /**
@@ -169,7 +170,7 @@ function filterHeadersForMatching (headers, headerFilters, matchOptions = {}) {
       if (!match.has(headerKey)) continue
     }
 
-    filtered[headerKey] = value
+    setHeader(filtered, headerKey, value)
   }
 
   return filtered
@@ -198,7 +199,7 @@ function filterHeadersForStorage (headers, headerFilters, matchOptions = {}) {
     // Skip if in exclude list (for security)
     if (excludeSet.has(headerKey)) continue
 
-    filtered[headerKey] = value
+    setHeader(filtered, headerKey, value)
   }
 
   return filtered
diff --git a/lib/mock/snapshot-utils.js b/lib/mock/snapshot-utils.js
index a14b69c15d4..c40f2f1caa2 100644
--- a/lib/mock/snapshot-utils.js
+++ b/lib/mock/snapshot-utils.js
@@ -1,6 +1,7 @@
 'use strict'
 
 const { InvalidArgumentError } = require('../core/errors')
+const { setHeader } = require('../core/util')
 const { runtimeFeatures } = require('../util/runtime-features.js')
 
 /**
@@ -116,7 +117,7 @@ function normalizeHeaders (headers) {
         // Convert Buffers to strings if needed
         const keyStr = Buffer.isBuffer(key) ? key.toString() : key
         const valueStr = Buffer.isBuffer(value) ? value.toString() : value
-        normalizedHeaders[keyStr.toLowerCase()] = valueStr
+        setHeader(normalizedHeaders, keyStr.toLowerCase(), valueStr)
       }
     }
     return normalizedHeaders
@@ -126,7 +127,7 @@ function normalizeHeaders (headers) {
   if (headers && typeof headers === 'object') {
     for (const [key, value] of Object.entries(headers)) {
       if (key && typeof key === 'string') {
-        normalizedHeaders[key.toLowerCase()] = Array.isArray(value) ? value.join(', ') : String(value)
+        setHeader(normalizedHeaders, key.toLowerCase(), Array.isArray(value) ? value.join(', ') : String(value))
       }
     }
   }
diff --git a/lib/util/cache.js b/lib/util/cache.js
index 1fac28af5d9..c658ef817e9 100644
--- a/lib/util/cache.js
+++ b/lib/util/cache.js
@@ -4,7 +4,8 @@ const {
   safeHTTPMethods,
   pathHasQueryOrFragment,
   hasSafeIterator,
-  isValidHTTPToken
+  isValidHTTPToken,
+  setHeader
 } = require('../core/util')
 
 const { serializePathWithQuery } = require('../core/util')
@@ -166,15 +167,20 @@ function makeCacheKey (opts) {
 
 function appendHeader (headers, key, val) {
   const headerName = key.toLowerCase()
-  const current = headers[headerName]
+  // Reading `headers[headerName]` directly would resolve `__proto__` (and any
+  // other inherited name) through the prototype chain rather than report the
+  // header as absent.
+  const current = Object.hasOwn(headers, headerName)
+    ? headers[headerName]
+    : undefined
   const values = Array.isArray(val) ? val : [val]
 
   if (current === undefined) {
-    headers[headerName] = Array.isArray(val) ? val.slice() : val
+    setHeader(headers, headerName, Array.isArray(val) ? val.slice() : val)
   } else if (Array.isArray(current)) {
     current.push(...values)
   } else {
-    headers[headerName] = [current, ...values]
+    setHeader(headers, headerName, [current, ...values])
   }
 }
 
@@ -692,7 +698,7 @@ function makeDeduplicationKey (cacheKey, excludeHeaders) {
       if (excludeHeaders?.has(header.toLowerCase())) {
         continue
       }
-      headers[header] = cacheKey.headers[header]
+      setHeader(headers, header, cacheKey.headers[header])
     }
   }
 
diff --git a/lib/web/fetch/headers.js b/lib/web/fetch/headers.js
index 024d1989588..41e0e65c79d 100644
--- a/lib/web/fetch/headers.js
+++ b/lib/web/fetch/headers.js
@@ -3,7 +3,7 @@
 'use strict'
 
 const { kConstruct } = require('../../core/symbols')
-const { kEnumerableProperty } = require('../../core/util')
+const { kEnumerableProperty, setHeader } = require('../../core/util')
 const {
   iteratorMixin,
   isValidHeaderName,
@@ -320,7 +320,7 @@ class HeadersList {
 
     if (this.headersMap.size !== 0) {
       for (const { name, value } of this.headersMap.values()) {
-        headers[name] = value
+        setHeader(headers, name, value)
       }
     }
 
diff --git a/test/cache-interceptor/cache-utils.js b/test/cache-interceptor/cache-utils.js
index fed0586668e..4f8b271346d 100644
--- a/test/cache-interceptor/cache-utils.js
+++ b/test/cache-interceptor/cache-utils.js
@@ -138,3 +138,20 @@ test('normalizeHeaders throws on non-string key in flat array', (t) => {
     message: 'opts.headers is not a valid header map'
   })
 })
+
+test('normalizeHeaders keeps a header named __proto__ without reprototyping the result', (t) => {
+  const { strictEqual, deepStrictEqual } = tspl(t, { plan: 5 })
+
+  // JSON.parse is the everyday way an own `__proto__` key shows up, e.g.
+  // headers read from a config file or a request body.
+  const headers = normalizeHeaders({
+    headers: JSON.parse('{"__proto__":"a","x-real":"same"}')
+  })
+
+  deepStrictEqual(Object.keys(headers).sort(), ['__proto__', 'x-real'])
+  strictEqual(Object.getOwnPropertyDescriptor(headers, '__proto__').value, 'a')
+  strictEqual(headers['x-real'], 'same')
+  strictEqual(Object.getPrototypeOf(headers), Object.prototype)
+  // A header named `length` must not resolve through an array prototype.
+  strictEqual(headers.length, undefined)
+})
diff --git a/test/interceptors/deduplicate.js b/test/interceptors/deduplicate.js
index 0092c3029c0..c5054bd21eb 100644
--- a/test/interceptors/deduplicate.js
+++ b/test/interceptors/deduplicate.js
@@ -1338,6 +1338,26 @@ describe('Deduplicate Interceptor', () => {
     notStrictEqual(key1, key2)
   })
 
+  test('makeDeduplicationKey does not collide on a header named __proto__', () => {
+    const withProto = JSON.parse('{"__proto__":"a","x-real":"same"}')
+
+    const key1 = makeDeduplicationKey({
+      origin: 'https://example.com',
+      method: 'GET',
+      path: '/',
+      headers: withProto
+    })
+
+    const key2 = makeDeduplicationKey({
+      origin: 'https://example.com',
+      method: 'GET',
+      path: '/',
+      headers: { 'x-real': 'same' }
+    })
+
+    notStrictEqual(key1, key2)
+  })
+
   test('makeDeduplicationKey produces same key for identical headers', () => {
     const key1 = makeDeduplicationKey({
       origin: 'https://example.com',
diff --git a/test/prototype-headers.js b/test/prototype-headers.js
index aa1bf15be26..74922c18084 100644
--- a/test/prototype-headers.js
+++ b/test/prototype-headers.js
@@ -82,3 +82,87 @@ test('request handles response trailers that shadow Object.prototype', async (t)
   assert.strictEqual(Object.getOwnPropertyDescriptor(trailers, '__proto__').value, 'trailer')
   assert.strictEqual(Object.getOwnPropertyDescriptor(trailers, 'constructor').value, 'built-in-trailer')
 })
+
+test('fetch sends a request header named __proto__', async (t) => {
+  const { createServer } = require('node:http')
+  const { fetch, Headers } = require('..')
+
+  let rawHeaders = null
+  const server = createServer((req, res) => {
+    rawHeaders = req.rawHeaders
+    res.end('OK')
+  })
+
+  t.after(() => {
+    server.closeAllConnections?.()
+    server.close()
+  })
+
+  await promisify(server.listen.bind(server))(0)
+
+  const headers = new Headers()
+  headers.set('__proto__', 'pwned')
+  headers.set('x-control', 'sent')
+
+  const response = await fetch(`http://localhost:${server.address().port}/`, {
+    headers
+  })
+  await response.text()
+
+  const received = {}
+  for (let i = 0; i < rawHeaders.length; i += 2) {
+    Object.defineProperty(received, rawHeaders[i].toLowerCase(), {
+      configurable: true,
+      enumerable: true,
+      value: rawHeaders[i + 1],
+      writable: true
+    })
+  }
+
+  assert.strictEqual(
+    Object.getOwnPropertyDescriptor(received, 'x-control').value,
+    'sent'
+  )
+  assert.strictEqual(
+    Object.getOwnPropertyDescriptor(received, '__proto__')?.value,
+    'pwned'
+  )
+})
+
+test('h2 sends a request header named __proto__', async (t) => {
+  const { createSecureServer } = require('node:http2')
+  const { once } = require('node:events')
+  const pem = require('@metcoder95/https-pem')
+
+  let received = null
+  const server = createSecureServer(await pem.generate({ opts: { keySize: 2048 } }))
+
+  server.on('stream', (stream, headers) => {
+    received = headers
+    stream.respond({ ':status': 200 })
+    stream.end('OK')
+  })
+
+  t.after(() => server.close())
+  await once(server.listen(0), 'listening')
+
+  const client = new Client(`https://localhost:${server.address().port}`, {
+    allowH2: true,
+    connect: { rejectUnauthorized: false }
+  })
+  t.after(() => client.close())
+
+  const { body } = await client.request({
+    path: '/',
+    method: 'GET',
+    // The flat array form is what buildRequestHeaders receives.
+    headers: ['__proto__', 'pwned', 'x-control', 'sent']
+  })
+  await body.text()
+
+  assert.strictEqual(received['x-control'], 'sent')
+  assert.strictEqual(
+    Object.getOwnPropertyDescriptor(received, '__proto__')?.value,
+    'pwned'
+  )
+})
diff --git a/test/snapshot-recorder.js b/test/snapshot-recorder.js
index 55fa38c747e..469213be567 100644
--- a/test/snapshot-recorder.js
+++ b/test/snapshot-recorder.js
@@ -422,3 +422,31 @@ test('SnapshotRecorder - redirect responses are stored correctly', (t) => {
   assert.strictEqual(snapshot.responses[0].statusCode, 302, 'First response should be redirect')
   assert.strictEqual(snapshot.responses[1].statusCode, 200, 'Second response should be final')
 })
+
+test('SnapshotRecorder - a header named __proto__ does not collide with its absence', (t) => {
+  const filters = createHeaderFilters({})
+
+  // JSON.parse is the everyday way an own `__proto__` key appears.
+  const withProto = formatRequestKey({
+    origin: 'https://example.com',
+    path: '/resource',
+    method: 'GET',
+    headers: JSON.parse('{"__proto__":"a","x-real":"same"}')
+  }, filters)
+
+  const withoutProto = formatRequestKey({
+    origin: 'https://example.com',
+    path: '/resource',
+    method: 'GET',
+    headers: { 'x-real': 'same' }
+  }, filters)
+
+  assert.strictEqual(
+    Object.getOwnPropertyDescriptor(withProto.headers, '__proto__')?.value,
+    'a'
+  )
+  assert.notStrictEqual(
+    createRequestHash(withProto),
+    createRequestHash(withoutProto)
+  )
+})