diff --git a/src/h2/stream.py b/src/h2/stream.py
index 249f73e0c..d0557cbc9 100644
--- a/src/h2/stream.py
+++ b/src/h2/stream.py
@@ -1094,7 +1094,17 @@ def receive_headers(self,
             ).stream_ended = cast("StreamEnded", es_events[0])
             events += es_events
 
-        self._initialize_content_length(headers)
+        # Content-Length is a header-block field. A trailers block must not
+        # reset the expected length established by the request or response.
+        if isinstance(headers_event, TrailersReceived):
+            if end_stream:
+                self._track_content_length(0, True)
+        else:
+            self._initialize_content_length(headers)
+            if end_stream:
+                # END_STREAM on the header block means there is no DATA to
+                # satisfy a declared content-length.
+                self._track_content_length(0, True)
 
         if isinstance(headers_event, TrailersReceived) and not end_stream:
             msg = "Trailers must have END_STREAM set"
diff --git a/tests/test_content_length_end_stream.py b/tests/test_content_length_end_stream.py
new file mode 100644
index 000000000..9f6ad8e1a
--- /dev/null
+++ b/tests/test_content_length_end_stream.py
@@ -0,0 +1,79 @@
+"""Content-Length must be satisfied when END_STREAM rides on a header block."""
+
+from __future__ import annotations
+
+import pytest
+
+import h2.config
+import h2.connection
+import h2.events
+import h2.exceptions
+
+REQUEST_HEADERS = [
+    (b":authority", b"example.com"),
+    (b":path", b"/"),
+    (b":scheme", b"https"),
+    (b":method", b"POST"),
+]
+
+
+def _connection() -> h2.connection.H2Connection:
+    connection = h2.connection.H2Connection()
+    connection.initiate_connection()
+    return connection
+
+
+def _pair() -> tuple[h2.connection.H2Connection, h2.connection.H2Connection]:
+    client = h2.connection.H2Connection()
+    client.initiate_connection()
+    server = h2.connection.H2Connection(config=h2.config.H2Configuration(client_side=False))
+    server.initiate_connection()
+    server.receive_data(client.data_to_send())
+    return client, server
+
+
+def test_request_content_length_rejects_end_stream_on_trailers() -> None:
+    client, server = _pair()
+    client.send_headers(1, REQUEST_HEADERS + [(b"content-length", b"5")])
+    server.receive_data(client.data_to_send())
+
+    client.send_headers(1, [(b"x-checksum", b"abc")], end_stream=True)
+    with pytest.raises(h2.exceptions.InvalidBodyLengthError):
+        server.receive_data(client.data_to_send())
+
+
+def test_request_content_length_accepts_matching_body_then_trailers() -> None:
+    client, server = _pair()
+    client.send_headers(1, REQUEST_HEADERS + [(b"content-length", b"5")])
+    server.receive_data(client.data_to_send())
+
+    client.send_data(1, b"hello")
+    server.receive_data(client.data_to_send())
+    client.send_headers(1, [(b"x-checksum", b"abc")], end_stream=True)
+    events = server.receive_data(client.data_to_send())
+
+    assert any(isinstance(event, h2.events.StreamEnded) for event in events)
+
+
+def test_response_content_length_rejects_end_stream_on_headers(frame_factory) -> None:
+    connection = _connection()
+    connection.send_headers(1, REQUEST_HEADERS, end_stream=True)
+
+    response = frame_factory.build_headers_frame(
+        [(b":status", b"200"), (b"content-length", b"5")],
+        flags=["END_STREAM"],
+    )
+    with pytest.raises(h2.exceptions.InvalidBodyLengthError):
+        connection.receive_data(response.serialize())
+
+
+def test_response_without_content_length_accepts_end_stream_on_headers(frame_factory) -> None:
+    connection = _connection()
+    connection.send_headers(1, REQUEST_HEADERS, end_stream=True)
+
+    response = frame_factory.build_headers_frame(
+        [(b":status", b"200")], flags=["END_STREAM"]
+    )
+    events = connection.receive_data(response.serialize())
+
+    assert any(isinstance(event, h2.events.StreamEnded) for event in events)