diff --git a/src/libraries/Common/tests/System/Net/Http/GenericLoopbackServer.cs b/src/libraries/Common/tests/System/Net/Http/GenericLoopbackServer.cs
index f4f92c0791c8f5..1ec1835d83a4ea 100644
--- a/src/libraries/Common/tests/System/Net/Http/GenericLoopbackServer.cs
+++ b/src/libraries/Common/tests/System/Net/Http/GenericLoopbackServer.cs
@@ -6,6 +6,7 @@
 using System.Text;
 using System.Threading.Tasks;
 using System.Security.Authentication;
+using System.Security.Cryptography.X509Certificates;
 using System.IO;
 using System.Net.Sockets;
 
@@ -93,6 +94,7 @@ public class GenericLoopbackOptions
     {
         public IPAddress Address { get; set; } = IPAddress.Loopback;
         public bool UseSsl { get; set; } = PlatformDetection.SupportsAlpn && !Capability.Http2ForceUnencryptedLoopback();
+        public X509Certificate2 Certificate { get; set; }
         public SslProtocols SslProtocols { get; set; } =
 #if !NETSTANDARD2_0 && !NETFRAMEWORK
                 SslProtocols.Tls13 |
diff --git a/src/libraries/Common/tests/System/Net/Http/HttpClientHandlerTest.ServerCertificates.cs b/src/libraries/Common/tests/System/Net/Http/HttpClientHandlerTest.ServerCertificates.cs
index d04b1d7aee6860..973a10967a452e 100644
--- a/src/libraries/Common/tests/System/Net/Http/HttpClientHandlerTest.ServerCertificates.cs
+++ b/src/libraries/Common/tests/System/Net/Http/HttpClientHandlerTest.ServerCertificates.cs
@@ -310,7 +310,6 @@ public async Task NoCallback_RevokedCertificate_RevocationChecking_Fails()
         public static readonly object[][] CertificateValidationServersAndExpectedPolicies =
         {
             new object[] { Configuration.Http.ExpiredCertRemoteServer, SslPolicyErrors.RemoteCertificateChainErrors },
-            new object[] { Configuration.Http.SelfSignedCertRemoteServer, SslPolicyErrors.RemoteCertificateChainErrors },
             new object[] { Configuration.Http.WrongHostNameCertRemoteServer , SslPolicyErrors.RemoteCertificateNameMismatch},
         };
 
@@ -365,6 +364,38 @@ public async Task UseCallback_BadCertificate_ExpectedPolicyErrors(string url, Ss
             }
         }
 
+        [Fact]
+        public async Task UseCallback_SelfSignedCertificate_ExpectedPolicyErrors()
+        {
+            using (HttpClientHandler handler = CreateHttpClientHandler())
+            using (HttpClient client = CreateHttpClient(handler))
+            {
+                bool callbackCalled = false;
+                X509Certificate2 certificate = TestHelper.CreateServerSelfSignedCertificate();
+
+                handler.ServerCertificateCustomValidationCallback = (request, cert, chain, errors) =>
+                {
+                    callbackCalled = true;
+                    Assert.NotNull(request);
+                    Assert.NotNull(cert);
+                    Assert.NotNull(chain);
+                    Assert.Equal(SslPolicyErrors.RemoteCertificateChainErrors, errors);
+                    return true;
+                };
+
+                var options = new LoopbackServer.Options { UseSsl = true, Certificate = certificate };
+
+                await LoopbackServer.CreateServerAsync(async (server, url) =>
+                {
+                    await TestHelper.WhenAllCompletedOrAnyFailed(
+                        server.AcceptConnectionSendResponseAndCloseAsync(),
+                        client.GetAsync($"https://{certificate.GetNameInfo(X509NameType.SimpleName, false)}:{url.Port}/"));
+                }, options);
+
+                Assert.True(callbackCalled);
+            }
+        }
+
         [OuterLoop("Uses external server")]
         [PlatformSpecific(TestPlatforms.Windows)] // CopyToAsync(Stream, TransportContext) isn't used on unix
         [Fact]
diff --git a/src/libraries/Common/tests/System/Net/Http/LoopbackServer.cs b/src/libraries/Common/tests/System/Net/Http/LoopbackServer.cs
index 47e1ec2540f819..f335a5d598cfe7 100644
--- a/src/libraries/Common/tests/System/Net/Http/LoopbackServer.cs
+++ b/src/libraries/Common/tests/System/Net/Http/LoopbackServer.cs
@@ -424,7 +424,7 @@ public static async Task<Connection> CreateAsync(Socket socket, Stream stream, O
                 if (httpOptions.UseSsl)
                 {
                     var sslStream = new SslStream(stream, false, delegate { return true; });
-                    using (X509Certificate2 cert = Configuration.Certificates.GetServerCertificate())
+                    using (X509Certificate2 cert = httpOptions.Certificate ?? Configuration.Certificates.GetServerCertificate())
                     {
                         await sslStream.AuthenticateAsServerAsync(
                             cert,
diff --git a/src/libraries/Common/tests/System/Net/Http/TestHelper.cs b/src/libraries/Common/tests/System/Net/Http/TestHelper.cs
index 041d6efe1e705f..163fdea225976e 100644
--- a/src/libraries/Common/tests/System/Net/Http/TestHelper.cs
+++ b/src/libraries/Common/tests/System/Net/Http/TestHelper.cs
@@ -118,5 +118,45 @@ public static byte[] GenerateRandomContent(int size)
             new Random(42).NextBytes(data);
             return data;
         }
+
+        public static X509Certificate2 CreateServerSelfSignedCertificate(string name = "localhost")
+        {
+            using (RSA root = RSA.Create())
+            {
+                CertificateRequest req = new CertificateRequest(
+                    $"CN={name}",
+                    root,
+                    HashAlgorithmName.SHA256,
+                    RSASignaturePadding.Pkcs1);
+
+                req.CertificateExtensions.Add(new X509BasicConstraintsExtension(true, false, 0, true));
+                req.CertificateExtensions.Add(new X509SubjectKeyIdentifierExtension(req.PublicKey, false));
+                req.CertificateExtensions.Add(new X509KeyUsageExtension(X509KeyUsageFlags.DigitalSignature | X509KeyUsageFlags.KeyEncipherment | X509KeyUsageFlags.DataEncipherment, false));
+                req.CertificateExtensions.Add(
+                    new X509EnhancedKeyUsageExtension(
+                            new OidCollection()
+                                {
+                                    new Oid("1.3.6.1.5.5.7.3.1", null),
+                                }, false));
+
+
+                SubjectAlternativeNameBuilder builder = new SubjectAlternativeNameBuilder();
+                builder.AddDnsName(name);
+                builder.AddIpAddress(IPAddress.Loopback);
+                builder.AddIpAddress(IPAddress.IPv6Loopback);
+                req.CertificateExtensions.Add(builder.Build());
+
+                DateTimeOffset start = DateTimeOffset.UtcNow.AddMinutes(-5);
+                DateTimeOffset end = start.AddMonths(1);
+
+                X509Certificate2 cert = req.CreateSelfSigned(start, end);
+                if (PlatformDetection.IsWindows)
+                {
+                    cert = new X509Certificate2(cert.Export(X509ContentType.Pfx));
+                }
+
+                return cert;
+            }
+        }
     }
 }