diff --git a/packages/playwright-core/src/server/fetch.ts b/packages/playwright-core/src/server/fetch.ts
index 444a86efb5..aef805798d 100644
--- a/packages/playwright-core/src/server/fetch.ts
+++ b/packages/playwright-core/src/server/fetch.ts
@@ -40,7 +40,7 @@ import { Tracing } from './trace/recorder/tracing';
 import type * as types from './types';
 import type { HeadersArray, ProxySettings } from './types';
 import { kMaxCookieExpiresDateInSeconds } from './network';
-import { clientCertificatesToTLSOptions } from './socksClientCertificatesInterceptor';
+import { clientCertificatesToTLSOptions, rewriteOpenSSLErrorIfNeeded } from './socksClientCertificatesInterceptor';
 
 type FetchRequestOptions = {
   userAgent: string;
@@ -452,7 +452,7 @@ export abstract class APIRequestContext extends SdkObject {
         body.on('data', chunk => chunks.push(chunk));
         body.on('end', notifyBodyFinished);
       });
-      request.on('error', reject);
+      request.on('error', error => reject(rewriteOpenSSLErrorIfNeeded(error)));
 
       const disposeListener = () => {
         reject(new Error('Request context disposed.'));
diff --git a/packages/playwright-core/src/server/socksClientCertificatesInterceptor.ts b/packages/playwright-core/src/server/socksClientCertificatesInterceptor.ts
index 13590579fe..17a4a708a6 100644
--- a/packages/playwright-core/src/server/socksClientCertificatesInterceptor.ts
+++ b/packages/playwright-core/src/server/socksClientCertificatesInterceptor.ts
@@ -22,7 +22,7 @@ import fs from 'fs';
 import tls from 'tls';
 import stream from 'stream';
 import { createSocket, createTLSSocket } from '../utils/happy-eyeballs';
-import { ManualPromise } from '../utils';
+import { ManualPromise, rewriteErrorMessage } from '../utils';
 import type { SocksSocketClosedPayload, SocksSocketDataPayload, SocksSocketRequestedPayload } from '../common/socksProxy';
 import { SocksProxy } from '../common/socksProxy';
 import type * as channels from '@protocol/channels';
@@ -150,8 +150,9 @@ class SocksProxyConnection {
         };
 
         const handleError = (error: Error) => {
-          debugLogger.log('client-certificates', `error when connecting to target: ${error.message}`);
-          const responseBody = 'Playwright client-certificate error: ' + error.message;
+          error = rewriteOpenSSLErrorIfNeeded(error);
+          debugLogger.log('client-certificates', `error when connecting to target: ${error.message.replaceAll('\n', ' ')}`);
+          const responseBody = 'Playwright client-certificate error: ' + error.message.replaceAll('\n', '<br>');
           if (internalTLS?.alpnProtocol === 'h2') {
             // This method is available only in Node.js 20+
             if ('performServerHandshake' in http2) {
@@ -297,3 +298,17 @@ export function clientCertificatesToTLSOptions(
 function rewriteToLocalhostIfNeeded(host: string): string {
   return host === 'local.playwright' ? 'localhost' : host;
 }
+
+export function rewriteOpenSSLErrorIfNeeded(error: Error): Error {
+  if (error.message !== 'unsupported')
+    return error;
+  return rewriteErrorMessage(error, [
+    'Unsupported TLS certificate.',
+    'Node.js (OpenSSL) has deprecated certifiates with the security algorithm of the given client-certifiate.',
+    'To fix this issue, you need to modernise the certificates by running the following command:',
+    'openssl pkcs12 -in oldPfxFile.pfx -nodes -legacy -out decryptedPfxFile.tmp',
+    'openssl pkcs12 -in decryptedPfxFile.tmp -export -out newPfxFile.pfx',
+    'Then, you can use the newPfxFile.pfx in your client-certificates configuration.',
+    'For more information, please refer to OpenSSL: https://github.com/openssl/openssl/blob/master/README-PROVIDERS.md#the-legacy-provider',
+  ].join('\n'));
+}
\ No newline at end of file
diff --git a/tests/assets/client-certificates/client/trusted/cert-legacy.pfx b/tests/assets/client-certificates/client/trusted/cert-legacy.pfx
new file mode 100644
index 0000000000..9f06aa35c8
Binary files /dev/null and b/tests/assets/client-certificates/client/trusted/cert-legacy.pfx differ
diff --git a/tests/library/client-certificates.spec.ts b/tests/library/client-certificates.spec.ts
index d54281b143..fd54f020a4 100644
--- a/tests/library/client-certificates.spec.ts
+++ b/tests/library/client-certificates.spec.ts
@@ -169,6 +169,51 @@ test.describe('fetch', () => {
     await request.dispose();
   });
 
+  test('pass with trusted client certificates in pfx format', async ({ playwright, startCCServer, asset }) => {
+    const serverURL = await startCCServer();
+    const request = await playwright.request.newContext({
+      ignoreHTTPSErrors: true,
+      clientCertificates: [{
+        origin: new URL(serverURL).origin,
+        pfxPath: asset('client-certificates/client/trusted/cert.pfx'),
+        passphrase: 'secure'
+      }],
+    });
+    const response = await request.get(serverURL);
+    expect(response.url()).toBe(serverURL);
+    expect(response.status()).toBe(200);
+    expect(await response.text()).toContain('Hello Alice, your certificate was issued by localhost!');
+    await request.dispose();
+  });
+
+  test('should throw a http error if the pfx passphrase is incorect', async ({ playwright, startCCServer, asset, browserName }) => {
+    const serverURL = await startCCServer({ useFakeLocalhost: browserName === 'webkit' && process.platform === 'darwin' });
+    const request = await playwright.request.newContext({
+      ignoreHTTPSErrors: true,
+      clientCertificates: [{
+        origin: new URL(serverURL).origin,
+        pfxPath: asset('client-certificates/client/trusted/cert.pfx'),
+        passphrase: 'this-password-is-incorrect'
+      }],
+    });
+    await expect(request.get(serverURL)).rejects.toThrow('mac verify failure');
+    await request.dispose();
+  });
+
+  test('should pass with matching certificates in legacy pfx format', async ({ playwright, startCCServer, asset, browserName }) => {
+    const serverURL = await startCCServer({ useFakeLocalhost: browserName === 'webkit' && process.platform === 'darwin' });
+    const request = await playwright.request.newContext({
+      ignoreHTTPSErrors: true,
+      clientCertificates: [{
+        origin: new URL(serverURL).origin,
+        pfxPath: asset('client-certificates/client/trusted/cert-legacy.pfx'),
+        passphrase: 'secure'
+      }],
+    });
+    await expect(request.get(serverURL)).rejects.toThrow('Unsupported TLS certificate');
+    await request.dispose();
+  });
+
   test('should work in the browser with request interception', async ({ browser, playwright, startCCServer, asset }) => {
     const serverURL = await startCCServer();
     const request = await playwright.request.newContext({
@@ -272,6 +317,21 @@ test.describe('browser', () => {
     await page.close();
   });
 
+  test('should pass with matching certificates in legacy pfx format', async ({ browser, startCCServer, asset, browserName }) => {
+    const serverURL = await startCCServer({ useFakeLocalhost: browserName === 'webkit' && process.platform === 'darwin' });
+    const page = await browser.newPage({
+      ignoreHTTPSErrors: true,
+      clientCertificates: [{
+        origin: new URL(serverURL).origin,
+        pfxPath: asset('client-certificates/client/trusted/cert-legacy.pfx'),
+        passphrase: 'secure'
+      }],
+    });
+    await page.goto(serverURL);
+    await expect(page.getByText('Unsupported TLS certificate.')).toBeVisible();
+    await page.close();
+  });
+
   test('should throw a http error if the pfx passphrase is incorect', async ({ browser, startCCServer, asset, browserName }) => {
     const serverURL = await startCCServer({ useFakeLocalhost: browserName === 'webkit' && process.platform === 'darwin' });
     const page = await browser.newPage({