diff --git a/lib/middleware/proxy.js b/lib/middleware/proxy.js
index 6b0fcf730..b2e0e7f63 100644
--- a/lib/middleware/proxy.js
+++ b/lib/middleware/proxy.js
@@ -3,6 +3,7 @@ const { Agent: httpAgent } = require('http')
 const { Agent: httpsAgent } = require('https')
 const httpProxy = require('http-proxy')
 const _ = require('lodash')
+const { lookup } = require('../utils/dns-utils')
 
 const log = require('../logger').create('proxy')
 
@@ -41,7 +42,10 @@ function parseProxyConfig (proxies, config) {
     const port = proxyDetails.port || defaultPorts[proxyDetails.protocol] || config.port
     const changeOrigin = proxyConfiguration.changeOrigin || false
     const Agent = protocol === 'https:' ? httpsAgent : httpAgent
-    const agent = new Agent({ keepAlive: true })
+    const agent = new Agent({
+      keepAlive: true,
+      lookup
+    })
     const proxy = httpProxy.createProxyServer({
       target: { host: hostname, port, protocol },
       xfwd: true,
diff --git a/lib/runner.js b/lib/runner.js
index 2e04065b6..fb67ebe92 100644
--- a/lib/runner.js
+++ b/lib/runner.js
@@ -7,6 +7,7 @@ const EventEmitter = require('events').EventEmitter
 const helper = require('./helper')
 const cfg = require('./config')
 const logger = require('./logger')
+const { lookup } = require('./utils/dns-utils')
 const log = logger.create('runner')
 
 function parseExitCode (buffer, defaultExitCode, failOnEmptyTestSuite) {
@@ -74,7 +75,8 @@ function run (cliOptionsOrConfig, done) {
     method: 'POST',
     headers: {
       'Content-Type': 'application/json'
-    }
+    },
+    lookup
   }
 
   const request = http.request(options, function (response) {
diff --git a/lib/stopper.js b/lib/stopper.js
index 964eb5e37..386fa5d83 100644
--- a/lib/stopper.js
+++ b/lib/stopper.js
@@ -2,6 +2,7 @@ const http = require('http')
 const cfg = require('./config')
 const logger = require('./logger')
 const helper = require('./helper')
+const { lookup } = require('./utils/dns-utils')
 
 exports.stop = function (cliOptionsOrConfig, done) {
   cliOptionsOrConfig = cliOptionsOrConfig || {}
@@ -42,7 +43,8 @@ exports.stop = function (cliOptionsOrConfig, done) {
     hostname: config.hostname,
     path: config.urlRoot + 'stop',
     port: config.port,
-    method: 'GET'
+    method: 'GET',
+    lookup
   })
 
   request.on('response', function (response) {
diff --git a/lib/utils/dns-utils.js b/lib/utils/dns-utils.js
new file mode 100644
index 000000000..5d281ed6f
--- /dev/null
+++ b/lib/utils/dns-utils.js
@@ -0,0 +1,11 @@
+const dns = require('dns')
+
+// Node >=17 has different DNS resolution (see
+// https://github.com/nodejs/node/issues/40702), it resolves domains
+// according to the OS settings instead of IPv4-address first. The Karma server
+// only listens on IPv4 address (127.0.0.1) by default, but the requests are
+// sent to `localhost` in several places and `localhost` is resolved into IPv6
+// address (`::`). So the run/stop/proxy request is unable to reach the Karma
+// server and produces an error. To mitigate this issue karma force the
+// IPv4-address first approach in Node >=17 as well.
+module.exports.lookup = (hostname, options, callback) => dns.lookup(hostname, { ...options, verbatim: false }, callback)
diff --git a/test/e2e/support/proxy.js b/test/e2e/support/proxy.js
index 5bf17c1fd..e78a4544c 100644
--- a/test/e2e/support/proxy.js
+++ b/test/e2e/support/proxy.js
@@ -8,7 +8,7 @@ module.exports = class Proxy {
     this.proxyPathRegExp = null
 
     this.proxy = httpProxy.createProxyServer({
-      target: 'http://localhost:9876'
+      target: 'http://127.0.0.1:9876'
     })
 
     this.proxy.on('error', (err) => {