diff --git a/lib/dispatcher/client-h1.js b/lib/dispatcher/client-h1.js
index a079e028e7f..fc4e0db9ec4 100644
--- a/lib/dispatcher/client-h1.js
+++ b/lib/dispatcher/client-h1.js
@@ -201,8 +201,6 @@ class Parser {
      * @param {*} llhttp
      */
   constructor (client, socket, { exports }) {
-    assert(Number.isFinite(client[kMaxHeadersSize]) && client[kMaxHeadersSize] > 0)
-
     this.llhttp = exports
     this.ptr = this.llhttp.llhttp_alloc(constants.TYPE.RESPONSE)
     this.client = client
diff --git a/lib/dispatcher/client.js b/lib/dispatcher/client.js
index 65380f19167..3939b89b5b4 100644
--- a/lib/dispatcher/client.js
+++ b/lib/dispatcher/client.js
@@ -1,5 +1,3 @@
-// @ts-check
-
 'use strict'
 
 const assert = require('node:assert')
@@ -60,6 +58,13 @@ const connectH2 = require('./client-h2.js')
 
 const kClosedResolve = Symbol('kClosedResolve')
 
+const getDefaultNodeMaxHeaderSize = http &&
+  http.maxHeaderSize &&
+  Number.isInteger(http.maxHeaderSize) &&
+  http.maxHeaderSize > 0
+  ? () => http.maxHeaderSize
+  : () => { throw new InvalidArgumentError('http module not available or http.maxHeaderSize invalid') }
+
 const noop = () => {}
 
 function getPipelining (client) {
@@ -123,8 +128,14 @@ class Client extends DispatcherBase {
       throw new InvalidArgumentError('unsupported maxKeepAliveTimeout, use keepAliveMaxTimeout instead')
     }
 
-    if (maxHeaderSize != null && !Number.isFinite(maxHeaderSize)) {
-      throw new InvalidArgumentError('invalid maxHeaderSize')
+    if (maxHeaderSize != null) {
+      if (!Number.isInteger(maxHeaderSize) || maxHeaderSize < 1) {
+        throw new InvalidArgumentError('invalid maxHeaderSize')
+      }
+    } else {
+      // If maxHeaderSize is not provided, use the default value from the http module
+      // or if that is not available, throw an error.
+      maxHeaderSize = getDefaultNodeMaxHeaderSize()
     }
 
     if (socketPath != null && typeof socketPath !== 'string') {
@@ -204,7 +215,7 @@ class Client extends DispatcherBase {
     this[kUrl] = util.parseOrigin(url)
     this[kConnector] = connect
     this[kPipelining] = pipelining != null ? pipelining : 1
-    this[kMaxHeadersSize] = maxHeaderSize || http.maxHeaderSize
+    this[kMaxHeadersSize] = maxHeaderSize
     this[kKeepAliveDefaultTimeout] = keepAliveTimeout == null ? 4e3 : keepAliveTimeout
     this[kKeepAliveMaxTimeout] = keepAliveMaxTimeout == null ? 600e3 : keepAliveMaxTimeout
     this[kKeepAliveTimeoutThreshold] = keepAliveTimeoutThreshold == null ? 2e3 : keepAliveTimeoutThreshold
diff --git a/test/client-errors.js b/test/client-errors.js
deleted file mode 100644
index 0c935d7cdac..00000000000
--- a/test/client-errors.js
+++ /dev/null
@@ -1,31 +0,0 @@
-'use strict'
-
-const { tspl } = require('@matteo.collina/tspl')
-const { test, after } = require('node:test')
-const { Client } = require('..')
-const net = require('node:net')
-
-// TODO: move to test/node-test/client-connect.js
-test('parser error', async (t) => {
-  t = tspl(t, { plan: 2 })
-
-  const server = net.createServer()
-  server.once('connection', (socket) => {
-    socket.write('asd\n\r213123')
-  })
-  after(() => server.close())
-
-  server.listen(0, () => {
-    const client = new Client(`http://localhost:${server.address().port}`)
-    after(() => client.destroy())
-
-    client.request({ path: '/', method: 'GET' }, (err) => {
-      t.ok(err)
-      client.close((err) => {
-        t.ifError(err)
-      })
-    })
-  })
-
-  await t.completed
-})
diff --git a/test/client-node-max-header-size.js b/test/client-node-max-header-size.js
index 379c5e6970a..4c23113dde8 100644
--- a/test/client-node-max-header-size.js
+++ b/test/client-node-max-header-size.js
@@ -41,4 +41,23 @@ describe("Node.js' --max-http-header-size cli option", () => {
 
     await t.completed
   })
+
+  test('--max-http-header-size with Client API', async (t) => {
+    t = tspl(t, { plan: 6 })
+    const command = 'node -e "new (require(\'.\').Client)(new URL(\'http://localhost:200\'))"'
+
+    exec(`${command} --max-http-header-size=0`, { stdio: 'pipe' }, (err, stdout, stderr) => {
+      t.strictEqual(err.code, 1)
+      t.strictEqual(stdout, '')
+      t.match(stderr, /http module not available or http.maxHeaderSize invalid/, '--max-http-header-size=0 should result in an Error when using the Client API')
+    })
+
+    exec(command, { stdio: 'pipe' }, (err, stdout, stderr) => {
+      t.ifError(err)
+      t.strictEqual(stdout, '')
+      t.strictEqual(stderr, '', 'default max-http-header-size should not throw')
+    })
+
+    await t.completed
+  })
 })
diff --git a/test/node-test/client-errors.js b/test/node-test/client-errors.js
index d53e9ffc146..39f04678dc6 100644
--- a/test/node-test/client-errors.js
+++ b/test/node-test/client-errors.js
@@ -1,12 +1,13 @@
 'use strict'
 
-const { test } = require('node:test')
 const assert = require('node:assert')
+const https = require('node:https')
+const net = require('node:net')
+const { Readable } = require('node:stream')
+const { test, after } = require('node:test')
 const { Client, Pool, errors } = require('../..')
 const { createServer } = require('node:http')
-const https = require('node:https')
 const pem = require('https-pem')
-const { Readable } = require('node:stream')
 const { tspl } = require('@matteo.collina/tspl')
 
 const { kSocket } = require('../../lib/core/symbols')
@@ -399,6 +400,46 @@ test('invalid options throws', (t, done) => {
     assert.strictEqual(err.message, 'invalid maxHeaderSize')
   }
 
+  try {
+    new Client(new URL('http://localhost:200'), { // eslint-disable-line
+      maxHeaderSize: 0
+    })
+    assert.ok(0)
+  } catch (err) {
+    assert.ok(err instanceof errors.InvalidArgumentError)
+    assert.strictEqual(err.message, 'invalid maxHeaderSize')
+  }
+
+  try {
+    new Client(new URL('http://localhost:200'), { // eslint-disable-line
+      maxHeaderSize: 0
+    })
+    assert.ok(0)
+  } catch (err) {
+    assert.ok(err instanceof errors.InvalidArgumentError)
+    assert.strictEqual(err.message, 'invalid maxHeaderSize')
+  }
+
+  try {
+    new Client(new URL('http://localhost:200'), { // eslint-disable-line
+      maxHeaderSize: -10
+    })
+    assert.ok(0)
+  } catch (err) {
+    assert.ok(err instanceof errors.InvalidArgumentError)
+    assert.strictEqual(err.message, 'invalid maxHeaderSize')
+  }
+
+  try {
+    new Client(new URL('http://localhost:200'), { // eslint-disable-line
+      maxHeaderSize: 1.5
+    })
+    assert.ok(0)
+  } catch (err) {
+    assert.ok(err instanceof errors.InvalidArgumentError)
+    assert.strictEqual(err.message, 'invalid maxHeaderSize')
+  }
+
   try {
     new Client(1) // eslint-disable-line
     assert.ok(0)
@@ -1324,3 +1365,27 @@ test('SocketError should expose socket details (tls)', async (t) => {
 
   await p.completed
 })
+
+test('parser error', async (t) => {
+  t = tspl(t, { plan: 2 })
+
+  const server = net.createServer()
+  server.once('connection', (socket) => {
+    socket.write('asd\n\r213123')
+  })
+  after(() => server.close())
+
+  server.listen(0, () => {
+    const client = new Client(`http://localhost:${server.address().port}`)
+    after(() => client.destroy())
+
+    client.request({ path: '/', method: 'GET' }, (err) => {
+      t.ok(err)
+      client.close((err) => {
+        t.ifError(err)
+      })
+    })
+  })
+
+  await t.completed
+})