diff --git a/samples/SelfHostServer/Startup.cs b/samples/SelfHostServer/Startup.cs
index 93251f2a1a..f4302222b9 100644
--- a/samples/SelfHostServer/Startup.cs
+++ b/samples/SelfHostServer/Startup.cs
@@ -47,7 +47,7 @@ namespace SelfHostServer
                 else
                 {
                     context.Response.ContentType = "text/plain";
-                    await context.Response.WriteAsync("Hello world");
+                    await context.Response.WriteAsync("Hello world from " + context.Request.Host + " at " + DateTime.Now);
                 }
             });
         }
diff --git a/src/Microsoft.Net.Http.Server/RequestProcessing/HeaderCollection.cs b/src/Microsoft.Net.Http.Server/RequestProcessing/HeaderCollection.cs
index 52eaa6e33b..4699dbd1e1 100644
--- a/src/Microsoft.Net.Http.Server/RequestProcessing/HeaderCollection.cs
+++ b/src/Microsoft.Net.Http.Server/RequestProcessing/HeaderCollection.cs
@@ -21,11 +21,15 @@ namespace Microsoft.Net.Http.Server
 
         private IDictionary<string, string[]> Store { get; set; }
 
+        // Readonly after the response has been sent.
+        internal bool Sent { get; set; }
+
         public string this[string key]
         {
             get { return Get(key); }
             set
             {
+                ThrowIfSent();
                 if (string.IsNullOrEmpty(value))
                 {
                     Remove(key);
@@ -40,7 +44,11 @@ namespace Microsoft.Net.Http.Server
         string[] IDictionary<string, string[]>.this[string key]
         {
             get { return Store[key]; }
-            set { Store[key] = value; }
+            set
+            {
+                ThrowIfSent();
+                Store[key] = value;
+            }
         }
 
         public int Count
@@ -50,7 +58,7 @@ namespace Microsoft.Net.Http.Server
 
         public bool IsReadOnly
         {
-            get { return false; }
+            get { return Sent; }
         }
 
         public ICollection<string> Keys
@@ -65,16 +73,19 @@ namespace Microsoft.Net.Http.Server
 
         public void Add(KeyValuePair<string, string[]> item)
         {
+            ThrowIfSent();
             Store.Add(item);
         }
 
         public void Add(string key, string[] value)
         {
+            ThrowIfSent();
             Store.Add(key, value);
         }
 
         public void Append(string key, string value)
         {
+            ThrowIfSent();
             string[] values;
             if (Store.TryGetValue(key, out values))
             {
@@ -91,6 +102,7 @@ namespace Microsoft.Net.Http.Server
 
         public void AppendValues(string key, params string[] values)
         {
+            ThrowIfSent();
             string[] oldValues;
             if (Store.TryGetValue(key, out oldValues))
             {
@@ -107,6 +119,7 @@ namespace Microsoft.Net.Http.Server
 
         public void Clear()
         {
+            ThrowIfSent();
             Store.Clear();
         }
 
@@ -152,21 +165,25 @@ namespace Microsoft.Net.Http.Server
 
         public bool Remove(KeyValuePair<string, string[]> item)
         {
+            ThrowIfSent();
             return Store.Remove(item);
         }
 
         public bool Remove(string key)
         {
+            ThrowIfSent();
             return Store.Remove(key);
         }
 
         public void Set(string key, string value)
         {
+            ThrowIfSent();
             Store[key] = new[] { value };
         }
 
         public void SetValues(string key, params string[] values)
         {
+            ThrowIfSent();
             Store[key] = values;
         }
 
@@ -179,5 +196,13 @@ namespace Microsoft.Net.Http.Server
         {
             return GetEnumerator();
         }
+
+        private void ThrowIfSent()
+        {
+            if (Sent)
+            {
+                throw new InvalidOperationException("The response headers cannot be modified because they have already been sent.");
+            }
+        }
     }
 }
\ No newline at end of file
diff --git a/src/Microsoft.Net.Http.Server/RequestProcessing/Response.cs b/src/Microsoft.Net.Http.Server/RequestProcessing/Response.cs
index 28ea172d40..b85010f985 100644
--- a/src/Microsoft.Net.Http.Server/RequestProcessing/Response.cs
+++ b/src/Microsoft.Net.Http.Server/RequestProcessing/Response.cs
@@ -583,6 +583,7 @@ namespace Microsoft.Net.Http.Server
 
         private List<GCHandle> SerializeHeaders(bool isOpaqueUpgrade)
         {
+            Headers.Sent = true; // Prohibit further modifications.
             UnsafeNclNativeMethods.HttpApi.HTTP_UNKNOWN_HEADER[] unknownHeaders = null;
             UnsafeNclNativeMethods.HttpApi.HTTP_RESPONSE_INFO[] knownHeaderInfo = null;
             List<GCHandle> pinnedHeaders;
diff --git a/test/Microsoft.AspNet.Server.WebListener.FunctionalTests/ResponseHeaderTests.cs b/test/Microsoft.AspNet.Server.WebListener.FunctionalTests/ResponseHeaderTests.cs
index c086ce3cea..66b18b3364 100644
--- a/test/Microsoft.AspNet.Server.WebListener.FunctionalTests/ResponseHeaderTests.cs
+++ b/test/Microsoft.AspNet.Server.WebListener.FunctionalTests/ResponseHeaderTests.cs
@@ -247,7 +247,7 @@ namespace Microsoft.AspNet.Server.WebListener
                     var body = responseInfo.Body;
                     body.Flush();
                     Assert.Throws<InvalidOperationException>(() => responseInfo.StatusCode = 404);
-                    responseHeaders.Add("Custom3", new string[] { "value3a, value3b", "value3c" }); // Ignored
+                    Assert.Throws<InvalidOperationException>(() => responseHeaders.Add("Custom3", new string[] { "value3a, value3b", "value3c" }));
                     return Task.FromResult(0);
                 }))
             {
@@ -277,7 +277,7 @@ namespace Microsoft.AspNet.Server.WebListener
                     var body = responseInfo.Body;
                     await body.FlushAsync();
                     Assert.Throws<InvalidOperationException>(() => responseInfo.StatusCode = 404);
-                    responseHeaders.Add("Custom3", new string[] { "value3a, value3b", "value3c" }); // Ignored
+                    Assert.Throws<InvalidOperationException>(() => responseHeaders.Add("Custom3", new string[] { "value3a, value3b", "value3c" }));
                 }))
             {
                 HttpResponseMessage response = await SendRequestAsync(address);
diff --git a/test/Microsoft.Net.Http.Server.FunctionalTests/OpaqueUpgradeTests.cs b/test/Microsoft.Net.Http.Server.FunctionalTests/OpaqueUpgradeTests.cs
index e3076cff0f..d6dc580fc2 100644
--- a/test/Microsoft.Net.Http.Server.FunctionalTests/OpaqueUpgradeTests.cs
+++ b/test/Microsoft.Net.Http.Server.FunctionalTests/OpaqueUpgradeTests.cs
@@ -24,7 +24,7 @@ namespace Microsoft.Net.Http.Server
                 byte[] body = Encoding.UTF8.GetBytes("Hello World");
                 context.Response.Body.Write(body, 0, body.Length);
 
-                context.Response.Headers["Upgrade"] = "WebSocket"; // Win8.1 blocks anything but WebSocket
+                Assert.Throws<InvalidOperationException>(() => context.Response.Headers["Upgrade"] = "WebSocket"); // Win8.1 blocks anything but WebSocket
                 await Assert.ThrowsAsync<InvalidOperationException>(async () => await context.UpgradeAsync());
                 context.Dispose();
                 HttpResponseMessage response = await clientTask;
diff --git a/test/Microsoft.Net.Http.Server.FunctionalTests/ResponseHeaderTests.cs b/test/Microsoft.Net.Http.Server.FunctionalTests/ResponseHeaderTests.cs
index 8b0dad5460..3059532f5d 100644
--- a/test/Microsoft.Net.Http.Server.FunctionalTests/ResponseHeaderTests.cs
+++ b/test/Microsoft.Net.Http.Server.FunctionalTests/ResponseHeaderTests.cs
@@ -233,8 +233,10 @@ namespace Microsoft.Net.Http.Server
                 responseHeaders.SetValues("Custom2", "value2a, value2b");
                 var body = context.Response.Body;
                 body.Flush();
-                Assert.Throws<InvalidOperationException>(() => context.Response.StatusCode = 404);
-                responseHeaders.Add("Custom3", new string[] { "value3a, value3b", "value3c" }); // Ignored
+                var ex = Assert.Throws<InvalidOperationException>(() => context.Response.StatusCode = 404);
+                Assert.Equal("Headers already sent.", ex.Message);
+                ex = Assert.Throws<InvalidOperationException>(() => responseHeaders.Add("Custom3", new string[] { "value3a, value3b", "value3c" }));
+                Assert.Equal("The response headers cannot be modified because they have already been sent.", ex.Message);
 
                 context.Dispose();
 
@@ -265,8 +267,10 @@ namespace Microsoft.Net.Http.Server
                 responseHeaders.SetValues("Custom2", "value2a, value2b");
                 var body = context.Response.Body;
                 await body.FlushAsync();
-                Assert.Throws<InvalidOperationException>(() => context.Response.StatusCode = 404);
-                responseHeaders.SetValues("Custom3", "value3a, value3b", "value3c"); // Ignored
+                var ex = Assert.Throws<InvalidOperationException>(() => context.Response.StatusCode = 404);
+                Assert.Equal("Headers already sent.", ex.Message);
+                ex = Assert.Throws<InvalidOperationException>(() => responseHeaders.Add("Custom3", new string[] { "value3a, value3b", "value3c" }));
+                Assert.Equal("The response headers cannot be modified because they have already been sent.", ex.Message);
 
                 context.Dispose();