diff --git a/src/Microsoft.AspNetCore.Server.Kestrel/KestrelServer.cs b/src/Microsoft.AspNetCore.Server.Kestrel/KestrelServer.cs
index 654544594b..04ece0d46d 100644
--- a/src/Microsoft.AspNetCore.Server.Kestrel/KestrelServer.cs
+++ b/src/Microsoft.AspNetCore.Server.Kestrel/KestrelServer.cs
@@ -247,6 +247,13 @@ namespace Microsoft.AspNetCore.Server.Kestrel
                 throw new InvalidOperationException(
                     $"Maximum request buffer size ({Options.Limits.MaxRequestBufferSize.Value}) must be greater than or equal to maximum request line size ({Options.Limits.MaxRequestLineSize}).");
             }
+
+            if (Options.Limits.MaxRequestBufferSize.HasValue &&
+                Options.Limits.MaxRequestBufferSize < Options.Limits.MaxRequestHeadersTotalSize)
+            {
+                throw new InvalidOperationException(
+                    $"Maximum request buffer size ({Options.Limits.MaxRequestBufferSize.Value}) must be greater than or equal to maximum request headers size ({Options.Limits.MaxRequestHeadersTotalSize}).");
+            }
         }
 
         private void StartLocalhost(KestrelEngine engine, ServerAddress parsedAddress)
diff --git a/test/Microsoft.AspNetCore.Server.Kestrel.FunctionalTests/MaxRequestBufferSizeTests.cs b/test/Microsoft.AspNetCore.Server.Kestrel.FunctionalTests/MaxRequestBufferSizeTests.cs
index 3c09271a4f..d60ae18dc4 100644
--- a/test/Microsoft.AspNetCore.Server.Kestrel.FunctionalTests/MaxRequestBufferSizeTests.cs
+++ b/test/Microsoft.AspNetCore.Server.Kestrel.FunctionalTests/MaxRequestBufferSizeTests.cs
@@ -6,9 +6,7 @@ using System.Collections.Generic;
 using System.IO;
 using System.Linq;
 using System.Net;
-using System.Net.Security;
 using System.Net.Sockets;
-using System.Security.Authentication;
 using System.Text;
 using System.Threading;
 using System.Threading.Tasks;
@@ -24,13 +22,22 @@ namespace Microsoft.AspNetCore.Server.Kestrel.FunctionalTests
     {
         private const int _dataLength = 20 * 1024 * 1024;
 
+        private static readonly string[] _requestLines = new[]
+        {
+            "POST / HTTP/1.0\r\n",
+            $"Content-Length: {_dataLength}\r\n",
+            "\r\n"
+        };
+
         public static IEnumerable<object[]> LargeUploadData
         {
             get
             {
                 var maxRequestBufferSizeValues = new Tuple<long?, bool>[] {
-                    // Smallest buffer that can hold a POST request line to the root.
-                    Tuple.Create((long?)"POST / HTTP/1.1\r\n".Length, true),
+                    // Smallest buffer that can hold a test request line without causing
+                    // the server to hang waiting for the end of the request line or
+                    // a header line.
+                    Tuple.Create((long?)(_requestLines.Max(line => line.Length)), true),
 
                     // Small buffer, but large enough to hold all request headers.
                     Tuple.Create((long?)16 * 1024, true),
@@ -186,6 +193,12 @@ namespace Microsoft.AspNetCore.Server.Kestrel.FunctionalTests
                     {
                         options.Limits.MaxRequestLineSize = (int)maxRequestBufferSize;
                     }
+
+                    if (maxRequestBufferSize.HasValue &&
+                        maxRequestBufferSize.Value < options.Limits.MaxRequestHeadersTotalSize)
+                    {
+                        options.Limits.MaxRequestHeadersTotalSize = (int)maxRequestBufferSize;
+                    }
                 })
                 .UseContentRoot(Directory.GetCurrentDirectory())
                 .Configure(app => app.Run(async context =>
@@ -246,9 +259,10 @@ namespace Microsoft.AspNetCore.Server.Kestrel.FunctionalTests
         {
             using (var writer = new StreamWriter(stream, Encoding.ASCII, bufferSize: 1024, leaveOpen: true))
             {
-                await writer.WriteAsync("POST / HTTP/1.0\r\n");
-                await writer.WriteAsync($"Content-Length: {contentLength}\r\n");
-                await writer.WriteAsync("\r\n");
+                foreach (var line in _requestLines)
+                {
+                    await writer.WriteAsync(line);
+                }
             }
         }
     }
diff --git a/test/Microsoft.AspNetCore.Server.KestrelTests/KestrelServerTests.cs b/test/Microsoft.AspNetCore.Server.KestrelTests/KestrelServerTests.cs
index 5225e5a16d..c22bdf6789 100644
--- a/test/Microsoft.AspNetCore.Server.KestrelTests/KestrelServerTests.cs
+++ b/test/Microsoft.AspNetCore.Server.KestrelTests/KestrelServerTests.cs
@@ -24,25 +24,30 @@ namespace Microsoft.AspNetCore.Server.KestrelTests
         public void StartWithNonPositiveThreadCountThrows(int threadCount)
         {
             var testLogger = new TestApplicationErrorLogger { ThrowOnCriticalErrors = false };
-            var server = CreateServer(new KestrelServerOptions() { ThreadCount = threadCount }, testLogger);
 
-            var exception = Assert.Throws<ArgumentOutOfRangeException>(() => StartDummyApplication(server));
+            using (var server = CreateServer(new KestrelServerOptions() { ThreadCount = threadCount }, testLogger))
+            {
+                var exception = Assert.Throws<ArgumentOutOfRangeException>(() => StartDummyApplication(server));
 
-            Assert.Equal("threadCount", exception.ParamName);
-            Assert.Equal(1, testLogger.CriticalErrorsLogged);
+                Assert.Equal("threadCount", exception.ParamName);
+                Assert.Equal(1, testLogger.CriticalErrorsLogged);
+            }
         }
 
         [Fact]
         public void StartWithInvalidAddressThrows()
         {
             var testLogger = new TestApplicationErrorLogger { ThrowOnCriticalErrors = false };
-            var server = CreateServer(new KestrelServerOptions(), testLogger);
-            server.Features.Get<IServerAddressesFeature>().Addresses.Add("http:/asdf");
 
-            var exception = Assert.Throws<FormatException>(() => StartDummyApplication(server));
+            using (var server = CreateServer(new KestrelServerOptions(), testLogger))
+            {
+                server.Features.Get<IServerAddressesFeature>().Addresses.Add("http:/asdf");
 
-            Assert.Contains("Invalid URL", exception.Message);
-            Assert.Equal(1, testLogger.CriticalErrorsLogged);
+                var exception = Assert.Throws<FormatException>(() => StartDummyApplication(server));
+
+                Assert.Contains("Invalid URL", exception.Message);
+                Assert.Equal(1, testLogger.CriticalErrorsLogged);
+            }
         }
 
         [Theory]
@@ -77,14 +82,37 @@ namespace Microsoft.AspNetCore.Server.KestrelTests
             options.Limits.MaxRequestBufferSize = maxRequestBufferSize;
             options.Limits.MaxRequestLineSize = maxRequestLineSize;
 
-            var server = CreateServer(options, testLogger);
+            using (var server = CreateServer(options, testLogger))
+            {
+                var exception = Assert.Throws<InvalidOperationException>(() => StartDummyApplication(server));
 
-            var exception = Assert.Throws<InvalidOperationException>(() => StartDummyApplication(server));
+                Assert.Equal(
+                    $"Maximum request buffer size ({maxRequestBufferSize}) must be greater than or equal to maximum request line size ({maxRequestLineSize}).",
+                    exception.Message);
+                Assert.Equal(1, testLogger.CriticalErrorsLogged);
+            }
+        }
 
-            Assert.Equal(
-                $"Maximum request buffer size ({maxRequestBufferSize}) must be greater than or equal to maximum request line size ({maxRequestLineSize}).",
-                exception.Message);
-            Assert.Equal(1, testLogger.CriticalErrorsLogged);
+        [Theory]
+        [InlineData(1, 2)]
+        [InlineData(int.MaxValue - 1, int.MaxValue)]
+        public void StartWithMaxRequestBufferSizeLessThanMaxRequestHeadersTotalSizeThrows(long maxRequestBufferSize, int maxRequestHeadersTotalSize)
+        {
+            var testLogger = new TestApplicationErrorLogger { ThrowOnCriticalErrors = false };
+            var options = new KestrelServerOptions();
+            options.Limits.MaxRequestBufferSize = maxRequestBufferSize;
+            options.Limits.MaxRequestLineSize = (int)maxRequestBufferSize;
+            options.Limits.MaxRequestHeadersTotalSize = maxRequestHeadersTotalSize;
+
+            using (var server = CreateServer(options, testLogger))
+            {
+                var exception = Assert.Throws<InvalidOperationException>(() => StartDummyApplication(server));
+
+                Assert.Equal(
+                    $"Maximum request buffer size ({maxRequestBufferSize}) must be greater than or equal to maximum request headers size ({maxRequestHeadersTotalSize}).",
+                    exception.Message);
+                Assert.Equal(1, testLogger.CriticalErrorsLogged);
+            }
         }
 
         [Fact]