diff --git a/src/client/Microsoft.Identity.Client/Internal/JsonWebToken.cs b/src/client/Microsoft.Identity.Client/Internal/JsonWebToken.cs
index 34a7322854..b060cd239c 100644
--- a/src/client/Microsoft.Identity.Client/Internal/JsonWebToken.cs
+++ b/src/client/Microsoft.Identity.Client/Internal/JsonWebToken.cs
@@ -127,10 +127,46 @@ private string CreateJsonPayload()
 
         public string Sign(X509Certificate2 certificate, bool sendX5C, bool useSha2AndPss)
         {
+            string encodedPayload = Base64UrlHelpers.EncodeString(CreateJsonPayload());
+
             // Base64Url encoded header and claims
-            string token = CreateJwtHeaderAndBody(certificate, sendX5C, useSha2AndPss);
+            string token = CreateJwtHeaderAndBody(
+                certificate,
+                sendX5C,
+                useSha2AndPss,
+                encodedPayload);
 
-            // Length check before sign
+            try
+            {
+                return SignToken(
+                    token,
+                    certificate,
+                    useSha2AndPss ?
+                        RSASignaturePadding.Pss :      // ESTS added support for PSS
+                        RSASignaturePadding.Pkcs1);    // Other IdPs may only support PKCS1
+            }
+            catch (CryptographicException) when (useSha2AndPss)
+            {
+                // Some private key providers do not support PSS. Retry with an RS256 header
+                // so the JWT algorithm and thumbprint remain consistent with PKCS#1 signing.
+                string fallbackToken = CreateJwtHeaderAndBody(
+                    certificate,
+                    sendX5C,
+                    useSha2AndPss: false,
+                    encodedPayload);
+
+                return SignToken(
+                    fallbackToken,
+                    certificate,
+                    RSASignaturePadding.Pkcs1);
+            }
+        }
+
+        private string SignToken(
+            string token,
+            X509Certificate2 certificate,
+            RSASignaturePadding signaturePadding)
+        {
             if (MaxTokenLength < token.Length)
             {
                 throw new MsalClientException(MsalError.EncodedTokenTooLong);
@@ -140,9 +176,7 @@ public string Sign(X509Certificate2 certificate, bool sendX5C, bool useSha2AndPs
             byte[] signature = _cryptographyManager.SignWithCertificate(
                 token,
                 certificate,
-                useSha2AndPss ?
-                    RSASignaturePadding.Pss :      // ESTS added support for PSS
-                    RSASignaturePadding.Pkcs1);    // Other IdPs may only support PKCS1
+                signaturePadding);
 
             return string.Concat(token, ".", Base64UrlHelpers.Encode(signature));
         }
@@ -206,15 +240,12 @@ private static string ComputeCertThumbprint(X509Certificate2 certificate, bool u
         private string CreateJwtHeaderAndBody(
             X509Certificate2 certificate,
             bool addX5C,
-            bool useSha2AndPss)
+            bool useSha2AndPss,
+            string encodedPayload)
         {
-
             string jsonHeader = CreateJsonHeader(certificate, addX5C, useSha2AndPss);
             string encodedHeader = Base64UrlHelpers.EncodeString(jsonHeader);
 
-            string jsonPayload = CreateJsonPayload();
-            string encodedPayload = Base64UrlHelpers.EncodeString(jsonPayload);
-
             return string.Concat(encodedHeader, ".", encodedPayload);
         }
     }
diff --git a/tests/Microsoft.Identity.Test.Unit/PublicApiTests/ClientCredentialWithCertTest.cs b/tests/Microsoft.Identity.Test.Unit/PublicApiTests/ClientCredentialWithCertTest.cs
index 3a0761a41d..71d0b1b5d2 100644
--- a/tests/Microsoft.Identity.Test.Unit/PublicApiTests/ClientCredentialWithCertTest.cs
+++ b/tests/Microsoft.Identity.Test.Unit/PublicApiTests/ClientCredentialWithCertTest.cs
@@ -10,6 +10,7 @@
 using System.Net.Http;
 using System.Security.Cryptography;
 using System.Security.Cryptography.X509Certificates;
+using System.Text;
 using System.Text.Json;
 using System.Threading;
 using System.Threading.Tasks;
@@ -24,6 +25,13 @@
 using Microsoft.Identity.Test.Common.Core.Mocks;
 using Microsoft.VisualStudio.TestTools.UnitTesting;
 using Microsoft.Identity.Client.Extensibility;
+using Microsoft.Identity.Client.Internal.Logger;
+using Microsoft.Identity.Client.PlatformsCommon.Interfaces;
+#if NETFRAMEWORK
+using Microsoft.Identity.Client.Platforms.netdesktop;
+#else
+using Microsoft.Identity.Client.Platforms.netstandard;
+#endif
 
 namespace Microsoft.Identity.Test.Unit
 {
@@ -658,6 +666,127 @@ public void ClientAssertionTests(bool sendX5C, bool useSha2AndPss, bool addExtra
             }
         }
 
+        [TestMethod]
+        public async Task AcquireTokenForClientWhenPssSigningFailsSendsRs256AssertionAsync()
+        {
+            // Arrange
+            using (var harness = CreateTestHarness())
+            using (RSA rsa = RSA.Create(2048))
+            using (X509Certificate2 certificate = new CertificateRequest(
+                "CN=PSS Fallback Test",
+                rsa,
+                HashAlgorithmName.SHA256,
+                RSASignaturePadding.Pkcs1).CreateSelfSigned(
+                    DateTimeOffset.UtcNow.AddMinutes(-1),
+                    DateTimeOffset.UtcNow.AddDays(1)))
+            {
+                SetupMocks(harness.HttpManager);
+                var cryptographyManager = new PssFailingCryptographyManager();
+
+                var app = ConfidentialClientApplicationBuilder
+                    .Create(TestConstants.ClientId)
+                    .WithAuthority(new Uri(ClientApplicationBase.DefaultAuthority), true)
+                    .WithHttpManager(harness.HttpManager)
+                    .WithPlatformProxy(new PssFailingPlatformProxy(cryptographyManager))
+                    .WithCertificate(certificate)
+                    .BuildConcrete();
+
+                MockHttpMessageHandler handler = CreateTokenResponseHttpHandler(clientCredentialFlow: true);
+                handler.AdditionalRequestValidation = request =>
+                {
+                    string requestContent = request.Content.ReadAsStringAsync().GetAwaiter().GetResult();
+                    IDictionary<string, string> formData = CoreHelpers.ParseKeyValueList(
+                        requestContent,
+                        '&',
+                        true,
+                        null);
+
+                    Assert.IsTrue(
+                        formData.TryGetValue(OAuth2Parameter.ClientAssertion, out string encodedAssertion),
+                        "Missing client_assertion from request.");
+
+                    var assertion = new JwtSecurityTokenHandler().ReadJwtToken(encodedAssertion);
+                    AssertClientAssertionHeader(
+                        certificate,
+                        assertion,
+                        sendX5c: true,
+                        useSha2AndPss: false);
+
+                    string[] assertionSegments = encodedAssertion.Split('.');
+                    Assert.HasCount(3, assertionSegments);
+
+                    byte[] signingInput = Encoding.UTF8.GetBytes(
+                        assertionSegments[0] + "." + assertionSegments[1]);
+                    byte[] signature = Base64UrlHelpers.DecodeBytes(assertionSegments[2]);
+
+                    using (RSA publicKey = certificate.GetRSAPublicKey())
+                    {
+                        Assert.IsTrue(
+                            publicKey.VerifyData(
+                                signingInput,
+                                signature,
+                                HashAlgorithmName.SHA256,
+                                RSASignaturePadding.Pkcs1),
+                            "The client_assertion signature should be valid RS256.");
+                    }
+                };
+
+                harness.HttpManager.AddMockHandler(handler);
+
+                // Act
+                AuthenticationResult result = await app
+                    .AcquireTokenForClient(TestConstants.s_scope)
+                    .WithSendX5C(true)
+                    .ExecuteAsync(CancellationToken.None)
+                    .ConfigureAwait(false);
+
+                // Assert
+                Assert.IsNotNull(result.AccessToken);
+                Assert.AreEqual(1, cryptographyManager.PssSigningAttempts);
+                Assert.AreEqual(1, cryptographyManager.Pkcs1SigningAttempts);
+            }
+        }
+
+#if NETFRAMEWORK
+        private sealed class PssFailingPlatformProxy : NetDesktopPlatformProxy
+#else
+        private sealed class PssFailingPlatformProxy : NetCorePlatformProxy
+#endif
+        {
+            private readonly ICryptographyManager _cryptographyManager;
+
+            public PssFailingPlatformProxy(ICryptographyManager cryptographyManager)
+                : base(new NullLogger())
+            {
+                _cryptographyManager = cryptographyManager;
+            }
+
+            protected override ICryptographyManager InternalGetCryptographyManager()
+                => _cryptographyManager;
+        }
+
+        private sealed class PssFailingCryptographyManager : CommonCryptographyManager
+        {
+            public int PssSigningAttempts { get; private set; }
+
+            public int Pkcs1SigningAttempts { get; private set; }
+
+            public override byte[] SignWithCertificate(
+                string message,
+                X509Certificate2 certificate,
+                RSASignaturePadding signaturePadding)
+            {
+                if (signaturePadding == RSASignaturePadding.Pss)
+                {
+                    PssSigningAttempts++;
+                    throw new CryptographicException("PSS signing is not supported by this key provider.");
+                }
+
+                Pkcs1SigningAttempts++;
+                return base.SignWithCertificate(message, certificate, signaturePadding);
+            }
+        }
+
         private static void AssertClientAssertionHeader(
             X509Certificate2 cert,
             JwtSecurityToken decodedToken,