diff --git a/CHANGES/8689.bugfix b/CHANGES/8689.bugfix
new file mode 100644
index 0000000000..809592d97c
--- /dev/null
+++ b/CHANGES/8689.bugfix
@@ -0,0 +1 @@
+Fixed ability to specify custom headers on a Remote.
diff --git a/pulpcore/download/factory.py b/pulpcore/download/factory.py
index dc2d75bb15..7babf0fa07 100644
--- a/pulpcore/download/factory.py
+++ b/pulpcore/download/factory.py
@@ -3,6 +3,7 @@
 import atexit
 import copy
 from gettext import gettext as _
+from multidict import MultiDict
 import platform
 from pkg_resources import get_distribution
 import ssl
@@ -15,8 +16,6 @@
 from .http import HttpDownloader
 from .file import FileDownloader
 
-import json
-
 
 PROTOCOL_MAP = {
     "http": HttpDownloader,
@@ -124,9 +123,13 @@ def _make_aiohttp_session_from_remote(self):
         if sslcontext:
             tcp_conn_opts["ssl_context"] = sslcontext
 
-        headers = {"User-Agent": user_agent()}
+        headers = MultiDict({"User-Agent": user_agent()})
         if self._remote.headers is not None:
-            headers.update(json.loads(self._remote.headers))
+            for header_dict in self._remote.headers:
+                user_agent_header = header_dict.pop("User-Agent", None)
+                if user_agent_header:
+                    headers["User-Agent"] = f"{headers['User-Agent']}, {user_agent_header}"
+                headers.extend(header_dict)
 
         conn = aiohttp.TCPConnector(**tcp_conn_opts)
         total = self._remote.total_timeout
diff --git a/pulpcore/tests/functional/api/using_plugin/test_crud_repos.py b/pulpcore/tests/functional/api/using_plugin/test_crud_repos.py
index 9ed11ca567..e0beda71e8 100644
--- a/pulpcore/tests/functional/api/using_plugin/test_crud_repos.py
+++ b/pulpcore/tests/functional/api/using_plugin/test_crud_repos.py
@@ -346,3 +346,14 @@ def test_delete(self):
         # verify the delete
         with self.assertRaises(ApiException):
             self.remotes_api.read(self.remote.pulp_href)
+
+    def test_headers(self):
+        # Test that headers value must be a list of dicts
+        data = {"headers": {"Connection": "keep-alive"}}
+        with self.assertRaises(ApiException):
+            self.remotes_api.partial_update(self.remote.pulp_href, data)
+        data = {"headers": [1, 2, 3]}
+        with self.assertRaises(ApiException):
+            self.remotes_api.partial_update(self.remote.pulp_href, data)
+        data = {"headers": [{"Connection": "keep-alive"}]}
+        self.remotes_api.partial_update(self.remote.pulp_href, data)
diff --git a/pulpcore/tests/functional/api/using_plugin/test_repo_versions.py b/pulpcore/tests/functional/api/using_plugin/test_repo_versions.py
index a593e6dd06..b1d24cf645 100644
--- a/pulpcore/tests/functional/api/using_plugin/test_repo_versions.py
+++ b/pulpcore/tests/functional/api/using_plugin/test_repo_versions.py
@@ -133,6 +133,7 @@ def test_02_sync_content(self):
         * The ``content_removed_summary`` attribute is correct.
         """
         body = gen_file_remote()
+        body.update({"headers": [{"Connection": "keep-alive"}]})
         self.remote.update(self.client.post(FILE_REMOTE_PATH, body))
         sync(self.cfg, self.remote, self.repo)
         repo = self.client.get(self.repo["pulp_href"])
diff --git a/pulpcore/tests/unit/download/test_factory.py b/pulpcore/tests/unit/download/test_factory.py
new file mode 100644
index 0000000000..089c370a8e
--- /dev/null
+++ b/pulpcore/tests/unit/download/test_factory.py
@@ -0,0 +1,33 @@
+from django.test import TestCase
+
+from pulpcore.download.factory import DownloaderFactory, user_agent
+from pulpcore.plugin.models import Remote
+
+
+class DownloaderFactoryHeadersTestCase(TestCase):
+    def test_user_agent_header(self):
+        remote = Remote.objects.create(url="http://example.org/", name="foo")
+        factory = DownloaderFactory(remote)
+        downloader = factory.build(remote.url)
+        default_user_agent = user_agent()
+        self.assertEqual(downloader.session.headers["User-Agent"], default_user_agent)
+        remote.delete()
+
+    def test_custom_user_agent_header(self):
+        remote = Remote.objects.create(
+            url="http://example.org/", headers=[{"User-Agent": "foo"}], name="foo"
+        )
+        factory = DownloaderFactory(remote)
+        downloader = factory.build(remote.url)
+        default_user_agent = user_agent()
+        expected_user_agent = f"{default_user_agent}, foo"
+        self.assertEqual(downloader.session.headers["User-Agent"], expected_user_agent)
+        remote.delete()
+
+    def test_custom_headers(self):
+        remote = Remote.objects.create(
+            url="http://example.org/", headers=[{"Connection": "keep-alive"}], name="foo"
+        )
+        factory = DownloaderFactory(remote)
+        downloader = factory.build(remote.url)
+        self.assertEqual(downloader.session.headers["Connection"], "keep-alive")