diff --git a/providers/slack/src/airflow/providers/slack/hooks/slack.py b/providers/slack/src/airflow/providers/slack/hooks/slack.py
index 63f74d0308b53..f2101d4320e40 100644
--- a/providers/slack/src/airflow/providers/slack/hooks/slack.py
+++ b/providers/slack/src/airflow/providers/slack/hooks/slack.py
@@ -18,6 +18,7 @@
 from __future__ import annotations
 
 import json
+import time
 import warnings
 from collections.abc import Sequence
 from functools import cached_property
@@ -28,7 +29,7 @@
 from slack_sdk.errors import SlackApiError
 from typing_extensions import NotRequired
 
-from airflow.exceptions import AirflowNotFoundException
+from airflow.exceptions import AirflowException, AirflowNotFoundException
 from airflow.hooks.base import BaseHook
 from airflow.providers.slack.utils import ConnectionExtraConfig
 from airflow.utils.helpers import exactly_one
@@ -291,7 +292,7 @@ def get_channel_id(self, channel_name: str) -> str:
         """
         next_cursor = None
         while not (channel_id := self._channels_mapping.get(channel_name)):
-            res = self.client.conversations_list(cursor=next_cursor, types="public_channel,private_channel")
+            res = self._call_conversations_list(cursor=next_cursor)
             if TYPE_CHECKING:
                 # Slack SDK response type too broad, this should make mypy happy
                 assert isinstance(res.data, dict)
@@ -308,6 +309,37 @@ def get_channel_id(self, channel_name: str) -> str:
             raise LookupError(msg)
         return channel_id
 
+    def _call_conversations_list(self, cursor: str | None = None):
+        """
+        Call ``conversations.list`` with automatic 429-retry.
+
+        .. versionchanged:: 3.0.0
+            Automatically retries on 429 responses (up to 5 times, honouring *Retry-After* header).
+
+        :param cursor: Pagination cursor returned by the previous ``conversations.list`` call.
+            Pass ``None`` (default) to start from the first page.
+        :raises AirflowException: If the method hits the rate-limit 5 times in a row.
+        :raises SlackApiError: Propagated when errors other than 429 occur.
+        :return: Slack SDK response for the page requested.
+        """
+        max_retries = 5
+        for attempt in range(max_retries):
+            try:
+                return self.client.conversations_list(cursor=cursor, types="public_channel,private_channel")
+            except SlackApiError as e:
+                if e.response.status_code == 429 and attempt < max_retries:
+                    retry_after = int(e.response.headers.get("Retry-After", 30))
+                    self.log.warning(
+                        "Rate limit hit. Retrying in %s seconds. Attempt %s/%s",
+                        retry_after,
+                        attempt + 1,
+                        max_retries,
+                    )
+                    time.sleep(retry_after)
+                else:
+                    raise
+        raise AirflowException("Max retries reached for conversations.list")
+
     def test_connection(self):
         """
         Tests the Slack API connection.
diff --git a/providers/slack/tests/unit/slack/hooks/test_slack.py b/providers/slack/tests/unit/slack/hooks/test_slack.py
index 73c44f426de3b..904ea02bf329f 100644
--- a/providers/slack/tests/unit/slack/hooks/test_slack.py
+++ b/providers/slack/tests/unit/slack/hooks/test_slack.py
@@ -26,7 +26,7 @@
 from slack_sdk.http_retry.builtin_handlers import ConnectionErrorRetryHandler, RateLimitErrorRetryHandler
 from slack_sdk.web.slack_response import SlackResponse
 
-from airflow.exceptions import AirflowNotFoundException
+from airflow.exceptions import AirflowException, AirflowNotFoundException
 from airflow.models.connection import Connection
 from airflow.providers.slack.hooks.slack import SlackHook
 
@@ -88,6 +88,13 @@ def fake_slack_response(*, data: dict | bytes, status_code: int = 200, **kwargs)
 
         return SlackResponse(status_code=status_code, data=data, **kwargs)
 
+    @staticmethod
+    def make_429():
+        resp = mock.MagicMock()
+        resp.status_code = 429
+        resp.headers = {"Retry-After": "1"}
+        return SlackApiError("ratelimited", response=resp)
+
     @pytest.mark.parametrize(
         "conn_id",
         [
@@ -389,6 +396,28 @@ def test_get_channel_id(self, mocked_client):
         with pytest.raises(LookupError, match="Unable to find slack channel"):
             hook.get_channel_id("troubleshooting")
 
+    def test_call_conversations_list_retries_then_succeeds(self, monkeypatch):
+        ok_resp = self.fake_slack_response(data={"channels": []})
+        monkeypatch.setattr(
+            "airflow.providers.slack.hooks.slack.WebClient",
+            lambda **_: mock.MagicMock(
+                conversations_list=mock.Mock(side_effect=[self.make_429(), self.make_429(), ok_resp])
+            ),
+        )
+        with mock.patch("time.sleep") as mocked_sleep:
+            hook = SlackHook(slack_conn_id=SLACK_API_DEFAULT_CONN_ID)
+            res = hook._call_conversations_list()
+            assert res is ok_resp
+            assert mocked_sleep.call_count == 2
+
+    def test_call_conversations_list_exceeds_max(self, monkeypatch):
+        monkeypatch.setattr(
+            "airflow.providers.slack.hooks.slack.WebClient",
+            lambda **_: mock.MagicMock(conversations_list=mock.Mock(side_effect=[self.make_429()] * 5)),
+        )
+        with pytest.raises(AirflowException, match="Max retries"):
+            SlackHook(slack_conn_id=SLACK_API_DEFAULT_CONN_ID)._call_conversations_list()
+
     def test_send_file_v2(self, mocked_client):
         SlackHook(slack_conn_id=SLACK_API_DEFAULT_CONN_ID).send_file_v2(
             channel_id="C00000000", file_uploads={"file": "/foo/bar/file.txt", "filename": "foo.txt"}