diff --git a/src/Servers/Kestrel/Core/src/Internal/Http/Http1UpgradeMessageBody.cs b/src/Servers/Kestrel/Core/src/Internal/Http/Http1UpgradeMessageBody.cs
index 8d67b56462c5..d75bb05d923d 100644
--- a/src/Servers/Kestrel/Core/src/Internal/Http/Http1UpgradeMessageBody.cs
+++ b/src/Servers/Kestrel/Core/src/Internal/Http/Http1UpgradeMessageBody.cs
@@ -14,6 +14,8 @@ namespace Microsoft.AspNetCore.Server.Kestrel.Core.Internal.Http
     /// </summary>
     internal sealed class Http1UpgradeMessageBody : Http1MessageBody
     {
+        private int _userCanceled;
+
         public Http1UpgradeMessageBody(Http1Connection context)
             : base(context)
         {
@@ -26,13 +28,13 @@ public Http1UpgradeMessageBody(Http1Connection context)
         public override ValueTask<ReadResult> ReadAsync(CancellationToken cancellationToken = default)
         {
             ThrowIfCompleted();
-            return _context.Input.ReadAsync(cancellationToken);
+            return ReadAsyncInternal(cancellationToken);
         }
 
         public override bool TryRead(out ReadResult result)
         {
             ThrowIfCompleted();
-            return _context.Input.TryRead(out result);
+            return TryReadInternal(out result);
         }
 
         public override void AdvanceTo(SequencePosition consumed)
@@ -54,6 +56,7 @@ public override void Complete(Exception exception)
 
         public override void CancelPendingRead()
         {
+            Interlocked.Exchange(ref _userCanceled, 1);
             _context.Input.CancelPendingRead();
         }
 
@@ -69,12 +72,49 @@ public override Task StopAsync()
 
         public override bool TryReadInternal(out ReadResult readResult)
         {
-            return _context.Input.TryRead(out readResult);
+            // Ignore the canceled readResult unless it was canceled by the user.
+            do
+            {
+                if (!_context.Input.TryRead(out readResult))
+                {
+                    return false;
+                }
+            } while (readResult.IsCanceled && Interlocked.Exchange(ref _userCanceled, 0) == 0);
+
+            return true;
         }
 
         public override ValueTask<ReadResult> ReadAsyncInternal(CancellationToken cancellationToken = default)
         {
-            return _context.Input.ReadAsync(cancellationToken);
+            ReadResult readResult;
+
+            // Ignore the canceled readResult unless it was canceled by the user.
+            do
+            {
+                var readTask = _context.Input.ReadAsync(cancellationToken);
+
+                if (!readTask.IsCompletedSuccessfully)
+                {
+                    return ReadAsyncInternalAwaited(readTask, cancellationToken);
+                }
+
+                readResult = readTask.GetAwaiter().GetResult();
+            } while (readResult.IsCanceled && Interlocked.Exchange(ref _userCanceled, 0) == 0);
+
+            return new ValueTask<ReadResult>(readResult);
+        }
+
+        private async ValueTask<ReadResult> ReadAsyncInternalAwaited(ValueTask<ReadResult> readTask, CancellationToken cancellationToken = default)
+        {
+            var readResult = await readTask;
+
+            // Ignore the canceled readResult unless it was canceled by the user.
+            while (readResult.IsCanceled && Interlocked.Exchange(ref _userCanceled, 0) == 0)
+            {
+                readResult = await _context.Input.ReadAsync(cancellationToken);
+            }
+
+            return readResult;
         }
     }
 }
diff --git a/src/Servers/Kestrel/test/InMemory.FunctionalTests/UpgradeTests.cs b/src/Servers/Kestrel/test/InMemory.FunctionalTests/UpgradeTests.cs
index cf36bb8a1512..cfd81233bee2 100644
--- a/src/Servers/Kestrel/test/InMemory.FunctionalTests/UpgradeTests.cs
+++ b/src/Servers/Kestrel/test/InMemory.FunctionalTests/UpgradeTests.cs
@@ -3,7 +3,10 @@
 
 using System;
 using System.IO;
+using System.IO.Pipelines;
 using System.Threading.Tasks;
+using Microsoft.AspNetCore.Connections;
+using Microsoft.AspNetCore.Connections.Features;
 using Microsoft.AspNetCore.Http.Features;
 using Microsoft.AspNetCore.Server.Kestrel.Core;
 using Microsoft.AspNetCore.Server.Kestrel.Core.Internal.Infrastructure;
@@ -343,5 +346,50 @@ await connection.Receive("HTTP/1.1 101 Switching Protocols",
                 await appCompletedTcs.Task.DefaultTimeout();
             }
         }
+
+        [Fact]
+        public async Task DoesNotThrowGivenCanceledReadResult()
+        {
+            var appCompletedTcs = new TaskCompletionSource<object>(TaskCreationOptions.RunContinuationsAsynchronously);
+
+            await using var server = new TestServer(async context =>
+            {
+                try
+                {
+                    var upgradeFeature = context.Features.Get<IHttpUpgradeFeature>();
+                    var duplexStream = await upgradeFeature.UpgradeAsync();
+
+                    // Kestrel will call Transport.Input.CancelPendingRead() during shutdown so idle connections
+                    // can wake up and shutdown gracefully. We manually call CancelPendingRead() to simulate this and
+                    // ensure the Stream returned by UpgradeAsync doesn't throw in this case.
+                    // https://github.com/dotnet/aspnetcore/issues/26482
+                    var connectionTransportFeature = context.Features.Get<IConnectionTransportFeature>();
+                    connectionTransportFeature.Transport.Input.CancelPendingRead();
+
+                    // Use ReadAsync() instead of CopyToAsync() for this test since IsCanceled is only checked in
+                    // HttpRequestStream.ReadAsync() and not HttpRequestStream.CopyToAsync() 
+                    Assert.Equal(0, await duplexStream.ReadAsync(new byte[1]));
+                    appCompletedTcs.SetResult(null);
+                }
+                catch (Exception ex)
+                {
+                    appCompletedTcs.SetException(ex);
+                    throw;
+                }
+            },
+            new TestServiceContext(LoggerFactory));
+
+            using (var connection = server.CreateConnection())
+            {
+                await connection.SendEmptyGetWithUpgrade();
+                await connection.Receive("HTTP/1.1 101 Switching Protocols",
+                    "Connection: Upgrade",
+                    $"Date: {server.Context.DateHeaderValue}",
+                    "",
+                    "");
+            }
+
+            await appCompletedTcs.Task.DefaultTimeout();
+        }
     }
 }