diff --git a/spec/std/http/server/handlers/compress_handler_spec.cr b/spec/std/http/server/handlers/compress_handler_spec.cr
index f6c0b5ab653d..cb4badc994d1 100644
--- a/spec/std/http/server/handlers/compress_handler_spec.cr
+++ b/spec/std/http/server/handlers/compress_handler_spec.cr
@@ -127,7 +127,7 @@ describe HTTP::CompressHandler do
     response.close
 
     io.rewind
-    io.to_s.should eq("HTTP/1.1 304 Not Modified\r\nContent-Length: 0\r\n\r\n")
+    io.to_s.should eq("HTTP/1.1 304 Not Modified\r\n\r\n")
   end
 
   it "don't try to compress upgraded response" do
diff --git a/spec/std/http/server/response_spec.cr b/spec/std/http/server/response_spec.cr
index 0042f40c008f..f22aed60b294 100644
--- a/spec/std/http/server/response_spec.cr
+++ b/spec/std/http/server/response_spec.cr
@@ -42,6 +42,40 @@ describe HTTP::Server::Response do
     io.to_s.should eq("HTTP/1.1 200 OK\r\nContent-Length: 0\r\n\r\n")
   end
 
+  it "does not automatically add the `content-length` header if the response is a 304" do
+    io = IO::Memory.new
+    response = Response.new(io)
+    response.status = :not_modified
+    response.close
+    io.to_s.should eq("HTTP/1.1 304 Not Modified\r\n\r\n")
+  end
+
+  it "does not automatically add the `content-length` header if the response is a 204" do
+    io = IO::Memory.new
+    response = Response.new(io)
+    response.status = :no_content
+    response.close
+    io.to_s.should eq("HTTP/1.1 204 No Content\r\n\r\n")
+  end
+
+  it "does not automatically add the `content-length` header if the response is informational" do
+    io = IO::Memory.new
+    response = Response.new(io)
+    response.status = :processing
+    response.close
+    io.to_s.should eq("HTTP/1.1 102 Processing\r\n\r\n")
+  end
+
+  # Case where the content-length represents the size of the data that would have been returned.
+  it "allows specifying the content-length header explicitly" do
+    io = IO::Memory.new
+    response = Response.new(io)
+    response.status = :not_modified
+    response.headers["Content-Length"] = "5"
+    response.close
+    io.to_s.should eq("HTTP/1.1 304 Not Modified\r\nContent-Length: 5\r\n\r\n")
+  end
+
   it "prints less then buffer's size" do
     io = IO::Memory.new
     response = Response.new(io)
diff --git a/src/http/server/response.cr b/src/http/server/response.cr
index a2651339fcca..8b6a5fab736a 100644
--- a/src/http/server/response.cr
+++ b/src/http/server/response.cr
@@ -223,7 +223,12 @@ class HTTP::Server
       def close
         return if closed?
 
-        if !response.wrote_headers? && !response.headers.has_key?("Content-Length")
+        # Conditionally determine based on status if the `content-length` header should be added automatically.
+        # See https://tools.ietf.org/html/rfc7230#section-3.3.2.
+        status = response.status
+        set_content_length = !(status.not_modified? || status.no_content? || status.informational?)
+
+        if !response.wrote_headers? && !response.headers.has_key?("Content-Length") && set_content_length
           response.content_length = @out_count
         end