diff --git a/Doc/library/http.client.rst b/Doc/library/http.client.rst
index f42afe91c58..649abd15873 100644
--- a/Doc/library/http.client.rst
+++ b/Doc/library/http.client.rst
@@ -362,6 +362,10 @@ server.  It provides access to the request headers and the entity
 body.  The response is an iterable object and can be used in a with
 statement.
 
+.. versionchanged:: 3.5
+   The :class:`io.BufferedIOBase` interface is now implemented and
+   all of its reader operations are supported.
+
 
 .. method:: HTTPResponse.read([amt])
 
diff --git a/Lib/http/client.py b/Lib/http/client.py
index 36e4e313105..80b0dcb7057 100644
--- a/Lib/http/client.py
+++ b/Lib/http/client.py
@@ -640,6 +640,8 @@ class HTTPResponse(io.BufferedIOBase):
             return b""
         if self.chunked:
             return self._read1_chunked(n)
+        if self.length is not None and (n < 0 or n > self.length):
+            n = self.length
         try:
             result = self.fp.read1(n)
         except ValueError:
@@ -650,6 +652,8 @@ class HTTPResponse(io.BufferedIOBase):
             result = self.fp.read1(16*1024)
         if not result and n:
             self._close_conn()
+        elif self.length is not None:
+            self.length -= len(result)
         return result
 
     def peek(self, n=-1):
@@ -667,9 +671,13 @@ class HTTPResponse(io.BufferedIOBase):
         if self.chunked:
             # Fallback to IOBase readline which uses peek() and read()
             return super().readline(limit)
+        if self.length is not None and (limit < 0 or limit > self.length):
+            limit = self.length
         result = self.fp.readline(limit)
         if not result and limit:
             self._close_conn()
+        elif self.length is not None:
+            self.length -= len(result)
         return result
 
     def _read1_chunked(self, n):
diff --git a/Lib/test/test_httplib.py b/Lib/test/test_httplib.py
index 295b9fb1468..6d2ed39ee9c 100644
--- a/Lib/test/test_httplib.py
+++ b/Lib/test/test_httplib.py
@@ -341,8 +341,8 @@ class BasicTest(TestCase):
         self.assertEqual(repr(exc), '''BadStatusLine("\'\'",)''')
 
     def test_partial_reads(self):
-        # if we have a length, the system knows when to close itself
-        # same behaviour than when we read the whole thing with read()
+        # if we have Content-Length, HTTPResponse knows when to close itself,
+        # the same behaviour as when we read the whole thing with read()
         body = "HTTP/1.1 200 Ok\r\nContent-Length: 4\r\n\r\nText"
         sock = FakeSocket(body)
         resp = client.HTTPResponse(sock)
@@ -355,9 +355,24 @@ class BasicTest(TestCase):
         resp.close()
         self.assertTrue(resp.closed)
 
+    def test_mixed_reads(self):
+        # readline() should update the remaining length, so that read() knows
+        # how much data is left and does not raise IncompleteRead
+        body = "HTTP/1.1 200 Ok\r\nContent-Length: 13\r\n\r\nText\r\nAnother"
+        sock = FakeSocket(body)
+        resp = client.HTTPResponse(sock)
+        resp.begin()
+        self.assertEqual(resp.readline(), b'Text\r\n')
+        self.assertFalse(resp.isclosed())
+        self.assertEqual(resp.read(), b'Another')
+        self.assertTrue(resp.isclosed())
+        self.assertFalse(resp.closed)
+        resp.close()
+        self.assertTrue(resp.closed)
+
     def test_partial_readintos(self):
-        # if we have a length, the system knows when to close itself
-        # same behaviour than when we read the whole thing with read()
+        # if we have Content-Length, HTTPResponse knows when to close itself,
+        # the same behaviour as when we read the whole thing with read()
         body = "HTTP/1.1 200 Ok\r\nContent-Length: 4\r\n\r\nText"
         sock = FakeSocket(body)
         resp = client.HTTPResponse(sock)
@@ -827,7 +842,7 @@ class BasicTest(TestCase):
         resp.begin()
         self.assertEqual(resp.read(), expected)
         # we should have reached the end of the file
-        self.assertEqual(sock.file.read(100), b"") #we read to the end
+        self.assertEqual(sock.file.read(), b"") #we read to the end
         resp.close()
 
     def test_chunked_sync(self):
@@ -839,19 +854,65 @@ class BasicTest(TestCase):
         resp.begin()
         self.assertEqual(resp.read(), expected)
         # the file should now have our extradata ready to be read
-        self.assertEqual(sock.file.read(100), extradata.encode("ascii")) #we read to the end
+        self.assertEqual(sock.file.read(), extradata.encode("ascii")) #we read to the end
         resp.close()
 
     def test_content_length_sync(self):
         """Check that we don't read past the end of the Content-Length stream"""
-        extradata = "extradata"
+        extradata = b"extradata"
         expected = b"Hello123\r\n"
-        sock = FakeSocket('HTTP/1.1 200 OK\r\nContent-Length: 10\r\n\r\nHello123\r\n' + extradata)
+        sock = FakeSocket(b'HTTP/1.1 200 OK\r\nContent-Length: 10\r\n\r\n' + expected + extradata)
         resp = client.HTTPResponse(sock, method="GET")
         resp.begin()
         self.assertEqual(resp.read(), expected)
         # the file should now have our extradata ready to be read
-        self.assertEqual(sock.file.read(100), extradata.encode("ascii")) #we read to the end
+        self.assertEqual(sock.file.read(), extradata) #we read to the end
+        resp.close()
+
+    def test_readlines_content_length(self):
+        extradata = b"extradata"
+        expected = b"Hello123\r\n"
+        sock = FakeSocket(b'HTTP/1.1 200 OK\r\nContent-Length: 10\r\n\r\n' + expected + extradata)
+        resp = client.HTTPResponse(sock, method="GET")
+        resp.begin()
+        self.assertEqual(resp.readlines(2000), [expected])
+        # the file should now have our extradata ready to be read
+        self.assertEqual(sock.file.read(), extradata) #we read to the end
+        resp.close()
+
+    def test_read1_content_length(self):
+        extradata = b"extradata"
+        expected = b"Hello123\r\n"
+        sock = FakeSocket(b'HTTP/1.1 200 OK\r\nContent-Length: 10\r\n\r\n' + expected + extradata)
+        resp = client.HTTPResponse(sock, method="GET")
+        resp.begin()
+        self.assertEqual(resp.read1(2000), expected)
+        # the file should now have our extradata ready to be read
+        self.assertEqual(sock.file.read(), extradata) #we read to the end
+        resp.close()
+
+    def test_readline_bound_content_length(self):
+        extradata = b"extradata"
+        expected = b"Hello123\r\n"
+        sock = FakeSocket(b'HTTP/1.1 200 OK\r\nContent-Length: 10\r\n\r\n' + expected + extradata)
+        resp = client.HTTPResponse(sock, method="GET")
+        resp.begin()
+        self.assertEqual(resp.readline(10), expected)
+        self.assertEqual(resp.readline(10), b"")
+        # the file should now have our extradata ready to be read
+        self.assertEqual(sock.file.read(), extradata) #we read to the end
+        resp.close()
+
+    def test_read1_bound_content_length(self):
+        extradata = b"extradata"
+        expected = b"Hello123\r\n"
+        sock = FakeSocket(b'HTTP/1.1 200 OK\r\nContent-Length: 30\r\n\r\n' + expected*3 + extradata)
+        resp = client.HTTPResponse(sock, method="GET")
+        resp.begin()
+        self.assertEqual(resp.read1(20), expected*2)
+        self.assertEqual(resp.read(), expected)
+        # the file should now have our extradata ready to be read
+        self.assertEqual(sock.file.read(), extradata) #we read to the end
         resp.close()
 
 class ExtendedReadTest(TestCase):
diff --git a/Misc/NEWS b/Misc/NEWS
index cbb1a5185a0..8338a840236 100644
--- a/Misc/NEWS
+++ b/Misc/NEWS
@@ -222,6 +222,10 @@ Core and Builtins
 Library
 -------
 
+- Issue #26499: Account for remaining Content-Length in
+  HTTPResponse.readline() and read1().  Based on patch by Silent Ghost.
+  Also document that HTTPResponse now supports these methods.
+
 - Issue #25320: Handle sockets in directories unittest discovery is scanning.
   Patch from Victor van den Elzen.