diff --git a/services/hackbot-api/app/slack/listeners/actions/start_agent_run.py b/services/hackbot-api/app/slack/listeners/actions/start_agent_run.py
index b405f089e70..e3060753dc0 100644
--- a/services/hackbot-api/app/slack/listeners/actions/start_agent_run.py
+++ b/services/hackbot-api/app/slack/listeners/actions/start_agent_run.py
@@ -73,6 +73,39 @@ def _generate_replacement_block(
     return {"type": "context", "elements": [{"type": "mrkdwn", "text": note}]}
 
 
+def _replace_in_actions_block(
+    block: dict, action: ButtonAction, note_block: dict
+) -> list[dict] | None:
+    """The blocks replacing an actions block once its clicked button is gone."""
+    elements = block["elements"]
+    filtered_elements = [e for e in elements if e["action_id"] != action.action_id]
+    if len(filtered_elements) == len(elements):
+        log.error(
+            "Clicked button '%s' is not in its block's elements, which is unexpected",
+            action.action_id,
+        )
+        return None
+    if not filtered_elements:
+        return [note_block]
+    return [{**block, "elements": filtered_elements}, note_block]
+
+
+def _replace_in_section_block(
+    block: dict, action: ButtonAction, note_block: dict
+) -> list[dict] | None:
+    """The blocks replacing a section once its clicked accessory button is gone."""
+    accessory = block.get("accessory")
+    if accessory is None or accessory.get("action_id") != action.action_id:
+        log.error(
+            "Clicked button '%s' is not its section's accessory, which is unexpected",
+            action.action_id,
+        )
+        return None
+    section = block.copy()
+    del section["accessory"]
+    return [section, note_block]
+
+
 def _message_with_note(
     message: dict, action: ButtonAction, note_block: dict
 ) -> dict | None:
@@ -85,26 +118,19 @@ def _message_with_note(
     for i, block in enumerate(blocks):
         if block["block_id"] != action.block_id:
             continue
-        if block["type"] != "actions":
+        if block["type"] == "actions":
+            replacement = _replace_in_actions_block(block, action, note_block)
+        elif block["type"] == "section":
+            replacement = _replace_in_section_block(block, action, note_block)
+        else:
             log.error(
-                "Clicked button '%s' is in a '%s' block, which is not supported yet",
+                "Clicked button '%s' is in a '%s' block, which is not supported",
                 action.action_id,
                 block["type"],
             )
             return None
-        elements = block["elements"]
-        filtered_elements = [e for e in elements if e["action_id"] != action.action_id]
-        if len(filtered_elements) == len(elements):
-            log.error(
-                "Clicked button '%s' is not in its block's elements, which is unexpected",
-                action.action_id,
-            )
+        if replacement is None:
             return None
-        replacement = (
-            [{**block, "elements": filtered_elements}, note_block]
-            if filtered_elements
-            else [note_block]
-        )
         return {
             "text": f"{message['text']}\n{note_block['elements'][0]['text']}".strip(),
             "blocks": blocks[:i] + replacement + blocks[i + 1 :],
diff --git a/services/hackbot-api/tests/test_slack_listeners.py b/services/hackbot-api/tests/test_slack_listeners.py
index 5e224a475b7..23a1ef63596 100644
--- a/services/hackbot-api/tests/test_slack_listeners.py
+++ b/services/hackbot-api/tests/test_slack_listeners.py
@@ -436,14 +436,31 @@ async def test_an_update_slack_refuses_is_logged_and_the_click_acknowledged(
         self.fake_ack.assert_awaited_once()
         assert "Slack said no" in caplog.text
 
-    async def test_a_button_outside_an_actions_block_is_logged_and_left(self, caplog):
-        # A button can also be a section's accessory, which is not supported yet.
+    async def test_a_section_accessory_button_is_replaced_with_the_note(self):
+        section = {
+            "type": "section",
+            "block_id": BLOCK_ID,
+            "text": {"type": "mrkdwn", "text": "Bug 1234"},
+            "accessory": _action(),
+        }
+        self.body["message"]["blocks"] = [section]
+
+        await self._call()
+
+        blocks = self._updated_blocks()
+        assert blocks[0] == {k: v for k, v in section.items() if k != "accessory"}
+        assert blocks[1]["type"] == "context"
+        assert "<@U0CLICKER>" in blocks[1]["elements"][0]["text"]
+        assert RUN_ID in blocks[1]["elements"][0]["text"]
+
+    async def test_a_section_whose_accessory_is_another_button_is_left(self, caplog):
+        other = {"type": "button", "action_id": "something_else", "value": "x"}
         self.body["message"]["blocks"] = [
             {
                 "type": "section",
                 "block_id": BLOCK_ID,
                 "text": {"type": "mrkdwn", "text": "Bug 1234"},
-                "accessory": _action(),
+                "accessory": other,
             }
         ]
 
@@ -451,7 +468,19 @@ async def test_a_button_outside_an_actions_block_is_logged_and_left(self, caplog
             await self._call()
 
         assert self._edits() == []
-        assert "'section' block" in caplog.text
+        assert "not its section's accessory" in caplog.text
+        self.fake_ack.assert_awaited_once()
+
+    async def test_a_button_in_an_unsupported_block_is_logged_and_left(self, caplog):
+        self.body["message"]["blocks"] = [
+            {"type": "input", "block_id": BLOCK_ID, "element": _action()}
+        ]
+
+        with caplog.at_level(logging.ERROR):
+            await self._call()
+
+        assert self._edits() == []
+        assert "'input' block" in caplog.text
         self.fake_ack.assert_awaited_once()
 
     async def test_a_message_without_the_button_is_left_alone(self):