diff --git a/doc/api/http2.md b/doc/api/http2.md
index 4663c7400b3730..19540a95a52a0d 100644
--- a/doc/api/http2.md
+++ b/doc/api/http2.md
@@ -2796,6 +2796,9 @@ Throws `ERR_INVALID_ARG_TYPE` for invalid `settings` argument.
 <!-- YAML
 added: v8.4.0
 changes:
+  - version: REPLACEME
+    pr-url: https://github.com/nodejs/node/pull/59917
+    description: Added the `strictSingleValueFields` option.
   - version: REPLACEME
     pr-url: https://github.com/nodejs/node/pull/61713
     description: Added `http1Options` option. The `Http1IncomingMessage`
@@ -2955,6 +2958,10 @@ changes:
     and trailing whitespace validation for HTTP/2 header field names and values
     as per [RFC-9113](https://www.rfc-editor.org/rfc/rfc9113.html#section-8.2.1).
     **Default:** `true`.
+  * `strictSingleValueFields` {boolean} If `true`, strict validation is used
+    for headers and trailers defined as having only a single value, such that
+    an error is thrown if multiple values are provided.
+    **Default:** `true`.
   * `...options` {Object} Any [`net.createServer()`][] option can be provided.
 * `onRequestHandler` {Function} See [Compatibility API][]
 * Returns: {Http2Server}
@@ -3012,6 +3019,9 @@ server.listen(8000);
 <!-- YAML
 added: v8.4.0
 changes:
+  - version: REPLACEME
+    pr-url: https://github.com/nodejs/node/pull/59917
+    description: Added the `strictSingleValueFields` option.
   - version: REPLACEME
     pr-url: https://github.com/nodejs/node/pull/61713
     description: Added `http1Options` option.
@@ -3133,6 +3143,10 @@ changes:
     and trailing whitespace validation for HTTP/2 header field names and values
     as per [RFC-9113](https://www.rfc-editor.org/rfc/rfc9113.html#section-8.2.1).
     **Default:** `true`.
+  * `strictSingleValueFields` {boolean} If `true`, strict validation is used
+    for headers and trailers defined as having only a single value, such that
+    an error is thrown if multiple values are provided.
+    **Default:** `true`.
   * `http1Options` {Object} An options object for configuring the HTTP/1
     fallback when `allowHTTP1` is `true`. These options are passed to the
     underlying HTTP/1 server. See [`http.createServer()`][] for available
diff --git a/lib/internal/http2/core.js b/lib/internal/http2/core.js
index 0b30abde1ea094..273ddd15414b51 100644
--- a/lib/internal/http2/core.js
+++ b/lib/internal/http2/core.js
@@ -136,6 +136,7 @@ const {
 const {
   assertIsObject,
   assertIsArray,
+  assertValidPseudoHeader,
   assertValidPseudoHeaderResponse,
   assertValidPseudoHeaderTrailer,
   assertWithinRange,
@@ -148,6 +149,7 @@ const {
   isPayloadMeaningless,
   kAuthority,
   kSensitiveHeaders,
+  kStrictSingleValueFields,
   kSocket,
   kRequest,
   kProtocol,
@@ -1318,6 +1320,8 @@ class Http2Session extends EventEmitter {
     this[kSocket] = socket;
     this[kTimeout] = null;
     this[kHandle] = undefined;
+    this[kStrictSingleValueFields] =
+      options.strictSingleValueFields;
 
     // Do not use nagle's algorithm
     if (typeof socket.setNoDelay === 'function')
@@ -2370,7 +2374,11 @@ class Http2Stream extends Duplex {
 
     this[kUpdateTimer]();
 
-    const headersList = buildNgHeaderString(headers, assertValidPseudoHeaderTrailer);
+    const headersList = buildNgHeaderString(
+      headers,
+      assertValidPseudoHeaderTrailer,
+      this.session[kStrictSingleValueFields],
+    );
     this[kSentTrailers] = headers;
 
     // Send the trailers in setImmediate so we don't do it on nghttp2 stack.
@@ -2579,7 +2587,11 @@ function prepareResponseHeaders(stream, headersParam, options) {
     stream[kSentHeaders] = headers;
   }
 
-  const headersList = buildNgHeaderString(headers, assertValidPseudoHeaderResponse);
+  const headersList = buildNgHeaderString(
+    headers,
+    assertValidPseudoHeaderResponse,
+    stream.session[kStrictSingleValueFields],
+  );
 
   return { headers, headersList, statusCode };
 }
@@ -2682,7 +2694,11 @@ function processRespondWithFD(self, fd, headers, offset = 0, length = -1,
 
   let headersList;
   try {
-    headersList = buildNgHeaderString(headers, assertValidPseudoHeaderResponse);
+    headersList = buildNgHeaderString(
+      headers,
+      assertValidPseudoHeaderResponse,
+      self.session[kStrictSingleValueFields],
+    );
   } catch (err) {
     if (self.ownsFd)
       tryClose(fd);
@@ -2909,7 +2925,11 @@ class ServerHttp2Stream extends Http2Stream {
     if (headers[HTTP2_HEADER_METHOD] === HTTP2_METHOD_HEAD)
       headRequest = options.endStream = true;
 
-    const headersList = buildNgHeaderString(headers);
+    const headersList = buildNgHeaderString(
+      headers,
+      assertValidPseudoHeader,
+      this.session[kStrictSingleValueFields],
+    );
 
     const streamOptions = options.endStream ? STREAM_OPTION_EMPTY_PAYLOAD : 0;
 
@@ -3173,7 +3193,11 @@ class ServerHttp2Stream extends Http2Stream {
 
     this[kUpdateTimer]();
 
-    const headersList = buildNgHeaderString(headers, assertValidPseudoHeaderResponse);
+    const headersList = buildNgHeaderString(
+      headers,
+      assertValidPseudoHeaderResponse,
+      this.session[kStrictSingleValueFields],
+    );
     if (!this[kInfoHeaders])
       this[kInfoHeaders] = [headers];
     else
@@ -3326,21 +3350,30 @@ function initializeOptions(options) {
   }
 
   if (options.maxSessionInvalidFrames !== undefined)
-    validateUint32(options.maxSessionInvalidFrames, 'maxSessionInvalidFrames');
+    validateUint32(options.maxSessionInvalidFrames, 'options.maxSessionInvalidFrames');
 
   if (options.maxSessionRejectedStreams !== undefined) {
     validateUint32(
       options.maxSessionRejectedStreams,
-      'maxSessionRejectedStreams',
+      'options.maxSessionRejectedStreams',
     );
   }
 
   if (options.unknownProtocolTimeout !== undefined)
-    validateUint32(options.unknownProtocolTimeout, 'unknownProtocolTimeout');
+    validateUint32(options.unknownProtocolTimeout, 'options.unknownProtocolTimeout');
   else
     // TODO(danbev): is this a good default value?
     options.unknownProtocolTimeout = 10000;
 
+  if (options.strictSingleValueFields !== undefined) {
+    validateBoolean(
+      options.strictSingleValueFields,
+      'options.strictSingleValueFields',
+    );
+  } else {
+    options.strictSingleValueFields = true;
+  }
+
 
   // Initialize http1Options bag for HTTP/1 fallback when allowHTTP1 is true.
   // This bag is passed to storeHTTPOptions() to configure HTTP/1 server
@@ -3553,6 +3586,15 @@ function connect(authority, options, listener) {
       throw new ERR_HTTP2_TOO_MANY_CUSTOM_SETTINGS();
   }
 
+  if (options.strictSingleValueFields !== undefined) {
+    validateBoolean(
+      options.strictSingleValueFields,
+      'options.strictSingleValueFields',
+    );
+  } else {
+    options.strictSingleValueFields = true;
+  }
+
   if (typeof authority === 'string')
     authority = new URL(authority);
 
diff --git a/lib/internal/http2/util.js b/lib/internal/http2/util.js
index ba981c8934dee9..25adc8f9697d82 100644
--- a/lib/internal/http2/util.js
+++ b/lib/internal/http2/util.js
@@ -39,6 +39,7 @@ const {
 
 const kAuthority = Symbol('authority');
 const kSensitiveHeaders = Symbol('sensitiveHeaders');
+const kStrictSingleValueFields = Symbol('strictSingleValueFields');
 const kSocket = Symbol('socket');
 const kProtocol = Symbol('protocol');
 const kProxySocket = Symbol('proxySocket');
@@ -121,7 +122,7 @@ const kValidPseudoHeaders = new SafeSet([
 
 // This set contains headers that are permitted to have only a single
 // value. Multiple instances must not be specified.
-const kSingleValueHeaders = new SafeSet([
+const kSingleValueFields = new SafeSet([
   HTTP2_HEADER_STATUS,
   HTTP2_HEADER_METHOD,
   HTTP2_HEADER_AUTHORITY,
@@ -690,6 +691,7 @@ function prepareRequestHeadersArray(headers, session) {
   const headersList = buildNgHeaderString(
     rawHeaders,
     assertValidPseudoHeader,
+    session[kStrictSingleValueFields],
   );
 
   return {
@@ -731,7 +733,11 @@ function prepareRequestHeadersObject(headers, session) {
       throw new ERR_HTTP2_CONNECT_PATH();
   }
 
-  const headersList = buildNgHeaderString(headersObject);
+  const headersList = buildNgHeaderString(
+    headersObject,
+    assertValidPseudoHeader,
+    session[kStrictSingleValueFields],
+  );
 
   return {
     headersObject,
@@ -751,10 +757,15 @@ const kNoHeaderFlags = StringFromCharCode(NGHTTP2_NV_FLAG_NONE);
  * format, rejecting illegal header configurations, and marking sensitive headers
  * that should not be indexed en route. This takes either a flat map of
  * raw headers ([k1, v1, k2, v2]) or a header object ({ k1: v1, k2: [v2, v3] }).
+ *
+ * Takes a validation function to check the pseudo-headers allowed for this
+ * message, and a boolean indicating whether to enforce strict single-value
+ * header validation.
  * @returns {[string, number]}
  */
 function buildNgHeaderString(arrayOrMap,
-                             assertValuePseudoHeader = assertValidPseudoHeader) {
+                             validatePseudoHeaderValue,
+                             strictSingleValueFields) {
   let headers = '';
   let pseudoHeaders = '';
   let count = 0;
@@ -765,7 +776,8 @@ function buildNgHeaderString(arrayOrMap,
 
   function processHeader(key, value) {
     key = key.toLowerCase();
-    const isSingleValueHeader = kSingleValueHeaders.has(key);
+    const isStrictSingleValueField = strictSingleValueFields &&
+      kSingleValueFields.has(key);
     let isArray = ArrayIsArray(value);
     if (isArray) {
       switch (value.length) {
@@ -776,13 +788,13 @@ function buildNgHeaderString(arrayOrMap,
           isArray = false;
           break;
         default:
-          if (isSingleValueHeader)
+          if (isStrictSingleValueField)
             throw new ERR_HTTP2_HEADER_SINGLE_VALUE(key);
       }
     } else {
       value = String(value);
     }
-    if (isSingleValueHeader) {
+    if (isStrictSingleValueField) {
       if (singles.has(key))
         throw new ERR_HTTP2_HEADER_SINGLE_VALUE(key);
       singles.add(key);
@@ -791,7 +803,7 @@ function buildNgHeaderString(arrayOrMap,
       kNeverIndexFlag :
       kNoHeaderFlags;
     if (key[0] === ':') {
-      const err = assertValuePseudoHeader(key);
+      const err = validatePseudoHeaderValue(key);
       if (err !== undefined)
         throw err;
       pseudoHeaders += `${key}\0${value}\0${flags}`;
@@ -893,7 +905,7 @@ function toHeaderObject(headers, sensitiveHeaders) {
     const existing = obj[name];
     if (existing === undefined) {
       obj[name] = name === HTTP2_HEADER_SET_COOKIE ? [value] : value;
-    } else if (!kSingleValueHeaders.has(name)) {
+    } else if (!kSingleValueFields.has(name)) {
       switch (name) {
         case HTTP2_HEADER_COOKIE:
           // https://tools.ietf.org/html/rfc7540#section-8.1.2.5
@@ -970,6 +982,7 @@ module.exports = {
   isPayloadMeaningless,
   kAuthority,
   kSensitiveHeaders,
+  kStrictSingleValueFields,
   kSocket,
   kProtocol,
   kProxySocket,
diff --git a/lib/internal/quic/quic.js b/lib/internal/quic/quic.js
index 459906d270dab6..026c0784f0bbe8 100644
--- a/lib/internal/quic/quic.js
+++ b/lib/internal/quic/quic.js
@@ -112,6 +112,7 @@ const {
 
 const {
   buildNgHeaderString,
+  assertValidPseudoHeader,
 } = require('internal/http2/util');
 
 const kEmptyObject = { __proto__: null };
@@ -887,8 +888,13 @@ class QuicStream {
     } else {
       debug(`stream ${this.id} sending headers`, headers);
     }
+    const headerString = buildNgHeaderString(
+      headers,
+      assertValidPseudoHeader,
+      true, // This could become an option in future
+    );
     // TODO(@jasnell): Support differentiating between early headers, primary headers, etc
-    return this.#handle.sendHeaders(1, buildNgHeaderString(headers), 1);
+    return this.#handle.sendHeaders(1, headerString, 1);
   }
 
   [kFinishClose](error) {
diff --git a/test/parallel/test-http2-single-headers-validation-disabled.js b/test/parallel/test-http2-single-headers-validation-disabled.js
new file mode 100644
index 00000000000000..4ea6da83673040
--- /dev/null
+++ b/test/parallel/test-http2-single-headers-validation-disabled.js
@@ -0,0 +1,53 @@
+'use strict';
+
+const common = require('../common');
+if (!common.hasCrypto)
+  common.skip('missing crypto');
+const assert = require('assert');
+const http2 = require('http2');
+
+const server = http2.createServer({
+  strictSingleValueFields: false
+});
+
+server.on('stream', common.mustCall((stream, _headers, _flags, rawHeaders) => {
+  assert.deepStrictEqual(rawHeaders.slice(8), [
+    'user-agent', 'abc',
+    'user-agent', 'xyz',
+    'referer', 'qwe',
+    'referer', 'asd',
+  ]);
+
+  stream.respond({
+    ':status': 200,
+    'expires': 'Thu, 01 Jan 1970 00:00:00 GMT',
+    'EXPIRES': 'Thu, 01 Jan 1970 00:00:00 GMT',
+    'content-type': ['a', 'b'],
+  });
+
+  stream.end();
+}));
+
+server.listen(0, common.mustCall(() => {
+  const client = http2.connect(`http://localhost:${server.address().port}`, {
+    strictSingleValueFields: false
+  });
+
+  const res = client.request({
+    'user-agent': 'abc',
+    'USER-AGENT': 'xyz',
+    'referer': ['qwe', 'asd'],
+  });
+
+  res.on('response', common.mustCall((_headers, _flags, rawHeaders) => {
+    assert.deepStrictEqual(rawHeaders.slice(2, 10), [
+      'expires', 'Thu, 01 Jan 1970 00:00:00 GMT',
+      'expires', 'Thu, 01 Jan 1970 00:00:00 GMT',
+      'content-type', 'a',
+      'content-type', 'b',
+    ]);
+
+    server.close();
+    client.close();
+  }));
+}));
diff --git a/test/parallel/test-http2-single-headers.js b/test/parallel/test-http2-single-headers-validation.js
similarity index 100%
rename from test/parallel/test-http2-single-headers.js
rename to test/parallel/test-http2-single-headers-validation.js
diff --git a/test/parallel/test-http2-util-assert-valid-pseudoheader.js b/test/parallel/test-http2-util-assert-valid-pseudoheader.js
index bd995f0338f106..29c41e7a5a83e9 100644
--- a/test/parallel/test-http2-util-assert-valid-pseudoheader.js
+++ b/test/parallel/test-http2-util-assert-valid-pseudoheader.js
@@ -4,20 +4,16 @@
 require('../common');
 const assert = require('assert');
 
-// Tests the assertValidPseudoHeader function that is used within the
-// buildNgHeaderString function. The assert function is not exported so we
-// have to test it through buildNgHeaderString
-
-const { buildNgHeaderString } = require('internal/http2/util');
+const { assertValidPseudoHeader } = require('internal/http2/util');
 
 // These should not throw
-buildNgHeaderString({ ':status': 'a' });
-buildNgHeaderString({ ':path': 'a' });
-buildNgHeaderString({ ':authority': 'a' });
-buildNgHeaderString({ ':scheme': 'a' });
-buildNgHeaderString({ ':method': 'a' });
+assertValidPseudoHeader(':status');
+assertValidPseudoHeader(':path');
+assertValidPseudoHeader(':authority');
+assertValidPseudoHeader(':scheme');
+assertValidPseudoHeader(':method');
 
-assert.throws(() => buildNgHeaderString({ ':foo': 'a' }), {
+assert.throws(() => assertValidPseudoHeader(':foo'), {
   code: 'ERR_HTTP2_INVALID_PSEUDOHEADER',
   name: 'TypeError',
   message: '":foo" is an invalid pseudoheader or is used incorrectly'
diff --git a/test/parallel/test-http2-util-headers-list.js b/test/parallel/test-http2-util-headers-list.js
index 0d1ac1d1b8c694..09135e865d4f98 100644
--- a/test/parallel/test-http2-util-headers-list.js
+++ b/test/parallel/test-http2-util-headers-list.js
@@ -9,6 +9,7 @@ if (!common.hasCrypto)
   common.skip('missing crypto');
 const assert = require('assert');
 const {
+  assertValidPseudoHeader,
   getAuthority,
   buildNgHeaderString,
   toHeaderObject
@@ -106,7 +107,7 @@ const {
   };
 
   assert.deepStrictEqual(
-    buildNgHeaderString(headers),
+    buildNgHeaderString(headers, assertValidPseudoHeader, true),
     [ [ ':path', 'abc\0', ':status', '200\0', 'abc', '1\0', 'xyz', '1\0',
         'xyz', '2\0', 'xyz', '3\0', 'xyz', '4\0', 'bar', '1\0', '' ].join('\0'),
       8 ]
@@ -123,7 +124,7 @@ const {
   };
 
   assert.deepStrictEqual(
-    buildNgHeaderString(headers),
+    buildNgHeaderString(headers, assertValidPseudoHeader, true),
     [ [ ':status', '200\0', ':path', 'abc\0', 'abc', '1\0', 'xyz', '1\0',
         'xyz', '2\0', 'xyz', '3\0', 'xyz', '4\0', '' ].join('\0'), 7 ]
   );
@@ -140,7 +141,7 @@ const {
   };
 
   assert.deepStrictEqual(
-    buildNgHeaderString(headers),
+    buildNgHeaderString(headers, assertValidPseudoHeader, true),
     [ [ ':status', '200\0', ':path', 'abc\0', 'abc', '1\0', 'xyz', '1\0',
         'xyz', '2\0', 'xyz', '3\0', 'xyz', '4\0', '' ].join('\0'), 7 ]
   );
@@ -156,7 +157,7 @@ const {
   headers[':path'] = 'abc';
 
   assert.deepStrictEqual(
-    buildNgHeaderString(headers),
+    buildNgHeaderString(headers, assertValidPseudoHeader, true),
     [ [ ':status', '200\0', ':path', 'abc\0', 'xyz', '1\0', 'xyz', '2\0',
         'xyz', '3\0', 'xyz', '4\0', '' ].join('\0'), 6 ]
   );
@@ -169,7 +170,7 @@ const {
     'set-cookie': ['foo=bar']
   };
   assert.deepStrictEqual(
-    buildNgHeaderString(headers),
+    buildNgHeaderString(headers, assertValidPseudoHeader, true),
     [ [ 'set-cookie', 'foo=bar\0', '' ].join('\0'), 1 ]
   );
 }
@@ -181,7 +182,7 @@ const {
     ':statuS': 204,
   };
 
-  assert.throws(() => buildNgHeaderString(headers), {
+  assert.throws(() => buildNgHeaderString(headers, assertValidPseudoHeader, true), {
     code: 'ERR_HTTP2_HEADER_SINGLE_VALUE',
     name: 'TypeError',
     message: 'Header field ":status" must only have a single value'
@@ -199,13 +200,14 @@ const {
   };
 
   assert.deepStrictEqual(
-    buildNgHeaderString(headers),
+    buildNgHeaderString(headers, assertValidPseudoHeader, true),
     [ ':status\x00200\x00\x00:path\x00abc\x00\x00abc\x001\x00\x00' +
       'xyz\x001\x00\x01xyz\x002\x00\x01xyz\x003\x00\x01xyz\x004\x00\x01', 7 ]
   );
 }
 
-// The following are not allowed to have multiple values
+// The following are not allowed to have multiple values by default, unless
+// strictSingleValueFields is set to false.
 [
   HTTP2_HEADER_STATUS,
   HTTP2_HEADER_METHOD,
@@ -248,10 +250,20 @@ const {
   HTTP2_HEADER_X_CONTENT_TYPE_OPTIONS,
 ].forEach((name) => {
   const msg = `Header field "${name}" must only have a single value`;
-  assert.throws(() => buildNgHeaderString({ [name]: [1, 2, 3] }), {
+  assert.throws(() => buildNgHeaderString(
+    { [name]: [1, 2, 3] },
+    assertValidPseudoHeader,
+    true
+  ), {
     code: 'ERR_HTTP2_HEADER_SINGLE_VALUE',
     message: msg
   });
+
+  assert(!(buildNgHeaderString(
+    { [name]: [1, 2, 3] },
+    assertValidPseudoHeader,
+    false
+  ) instanceof Error), name);
 });
 
 [
@@ -285,7 +297,11 @@ const {
   HTTP2_HEADER_WWW_AUTHENTICATE,
   HTTP2_HEADER_X_FRAME_OPTIONS,
 ].forEach((name) => {
-  assert(!(buildNgHeaderString({ [name]: [1, 2, 3] }) instanceof Error), name);
+  assert(!(buildNgHeaderString(
+    { [name]: [1, 2, 3] },
+    assertValidPseudoHeader,
+    true
+  ) instanceof Error), name);
 });
 
 [
@@ -304,7 +320,11 @@ const {
   'Proxy-Connection',
   'Keep-Alive',
 ].forEach((name) => {
-  assert.throws(() => buildNgHeaderString({ [name]: 'abc' }), {
+  assert.throws(() => buildNgHeaderString(
+    { [name]: 'abc' },
+    assertValidPseudoHeader,
+    true
+  ), {
     code: 'ERR_HTTP2_INVALID_CONNECTION_HEADERS',
     name: 'TypeError',
     message: 'HTTP/1 Connection specific headers are forbidden: ' +
@@ -312,7 +332,11 @@ const {
   });
 });
 
-assert.throws(() => buildNgHeaderString({ [HTTP2_HEADER_TE]: ['abc'] }), {
+assert.throws(() => buildNgHeaderString(
+  { [HTTP2_HEADER_TE]: ['abc'] },
+  assertValidPseudoHeader,
+  true
+), {
   code: 'ERR_HTTP2_INVALID_CONNECTION_HEADERS',
   name: 'TypeError',
   message: 'HTTP/1 Connection specific headers are forbidden: ' +
@@ -320,7 +344,11 @@ assert.throws(() => buildNgHeaderString({ [HTTP2_HEADER_TE]: ['abc'] }), {
 });
 
 assert.throws(
-  () => buildNgHeaderString({ [HTTP2_HEADER_TE]: ['abc', 'trailers'] }), {
+  () => buildNgHeaderString(
+    { [HTTP2_HEADER_TE]: ['abc', 'trailers'] },
+    assertValidPseudoHeader,
+    true
+  ), {
     code: 'ERR_HTTP2_INVALID_CONNECTION_HEADERS',
     name: 'TypeError',
     message: 'HTTP/1 Connection specific headers are forbidden: ' +
@@ -328,13 +356,25 @@ assert.throws(
   });
 
 // These should not throw
-buildNgHeaderString({ te: 'trailers' });
-buildNgHeaderString({ te: ['trailers'] });
+buildNgHeaderString(
+  { te: 'trailers' },
+  assertValidPseudoHeader,
+  true
+);
+buildNgHeaderString(
+  { te: ['trailers'] },
+  assertValidPseudoHeader,
+  true
+);
 
 // HTTP/2 encourages use of Host instead of :authority when converting
 // from HTTP/1 to HTTP/2, so we no longer disallow it.
 // Refs: https://github.com/nodejs/node/issues/29858
-buildNgHeaderString({ [HTTP2_HEADER_HOST]: 'abc' });
+buildNgHeaderString(
+  { [HTTP2_HEADER_HOST]: 'abc' },
+  assertValidPseudoHeader,
+  true
+);
 
 // If both are present, the latter has priority
 assert.strictEqual(getAuthority({