diff --git a/man/ostree.repo-config.xml b/man/ostree.repo-config.xml
index 8ae6ad42..388b9e62 100644
--- a/man/ostree.repo-config.xml
+++ b/man/ostree.repo-config.xml
@@ -122,6 +122,27 @@ Boston, MA 02111-1307, USA.
         keep free. The default value is 3.</para></listitem>
       </varlistentry>
 
+      <varlistentry>
+        <term><varname>add-remotes-config-dir</varname></term>
+        <listitem>
+          <para>
+            Boolean value controlling whether new remotes will be added
+            in the remotes configuration directory. Defaults to
+            <literal>true</literal> for system ostree repositories. When
+            this is <literal>false</literal>, remotes will be added in
+            the repository's <filename>config</filename> file.
+          </para>
+          <para>
+            This only applies to repositories that use a remotes
+            configuration directory such as system ostree repositories,
+            which use <filename>/etc/ostree/remotes.d</filename>.
+            Non-system repositories do not use a remotes configuration
+            directory unless one is specified when the repository is
+            opened.
+          </para>
+        </listitem>
+      </varlistentry>
+
     </variablelist>
   </refsect1>
 
diff --git a/src/libostree/ostree-repo-private.h b/src/libostree/ostree-repo-private.h
index fdcd8f3f..865cb120 100644
--- a/src/libostree/ostree-repo-private.h
+++ b/src/libostree/ostree-repo-private.h
@@ -154,6 +154,7 @@ struct OstreeRepo {
   gboolean generate_sizes;
   guint64 tmp_expiry_seconds;
   gchar *collection_id;
+  gboolean add_remotes_config_dir; /* Add new remotes in remotes.d dir */
 
   OstreeRepo *parent_repo;
 };
diff --git a/src/libostree/ostree-repo.c b/src/libostree/ostree-repo.c
index c0d4a8e7..b529854e 100644
--- a/src/libostree/ostree-repo.c
+++ b/src/libostree/ostree-repo.c
@@ -1010,11 +1010,12 @@ impl_repo_remote_add (OstreeRepo     *self,
 
   remote = ostree_remote_new (name);
 
-  /* Only add repos in remotes.d for system repos since that was the
-   * legacy behavior and non-system repos would not expect it.
+  /* Only add repos in remotes.d if the repo option
+   * add-remotes-config-dir is true. This is the default for system
+   * repos.
    */
   g_autoptr(GFile) etc_ostree_remotes_d = get_remotes_d_dir (self, sysroot);
-  if (etc_ostree_remotes_d && ostree_repo_is_system (self))
+  if (etc_ostree_remotes_d && self->add_remotes_config_dir)
     {
       g_autoptr(GError) local_error = NULL;
 
@@ -2231,6 +2232,17 @@ reload_core_config (OstreeRepo          *self,
         }
     }
 
+  /* By default, only add remotes in a remotes config directory for
+   * system repos. This is to preserve legacy behavior for non-system
+   * repos that specify a remotes config dir (flatpak).
+   */
+  { gboolean is_system = ostree_repo_is_system (self);
+
+    if (!ot_keyfile_get_boolean_with_default (self->config, "core", "add-remotes-config-dir",
+                                              is_system, &self->add_remotes_config_dir, error))
+      return FALSE;
+  }
+
   return TRUE;
 }
 
diff --git a/tests/admin-test.sh b/tests/admin-test.sh
index 805a7130..f5d33a6f 100644
--- a/tests/admin-test.sh
+++ b/tests/admin-test.sh
@@ -19,7 +19,7 @@
 
 set -euo pipefail
 
-echo "1..$((21 + ${extra_admin_tests:-0}))"
+echo "1..$((22 + ${extra_admin_tests:-0}))"
 
 function validate_bootloader() {
     cd ${test_tmpdir};
@@ -292,6 +292,15 @@ assert_not_file_has_content sysroot/ostree/repo/config remote-test-nonphysical
 assert_file_has_content ${deployment}/etc/ostree/remotes.d/remote-test-nonphysical.conf testos-repo
 echo "ok remote add nonphysical sysroot"
 
+# Test that setting add-remotes-config-dir to false adds a remote in the
+# config file rather than the remotes config dir even though this is a
+# "system" repo.
+${CMD_PREFIX} ostree --repo=sysroot/ostree/repo config set core.add-remotes-config-dir false
+${CMD_PREFIX} ostree --sysroot=${deployment} remote add --set=gpg-verify=false remote-test-config-dir file://$(pwd)/testos-repo
+assert_not_has_file ${deployment}/etc/ostree/remotes.d/remote-test-config-dir.conf testos-repo
+assert_file_has_content sysroot/ostree/repo/config remote-test-config-dir
+echo "ok remote add nonphysical sysroot add-remotes-config-dir false"
+
 if env OSTREE_SYSROOT_DEBUG="${OSTREE_SYSROOT_DEBUG},test-fifreeze" \
        ${CMD_PREFIX} ostree admin deploy --os=testos testos:testos/buildmaster/x86_64-runtime 2>err.txt; then
     fatal "fifreeze-test exited successfully?"
diff --git a/tests/test-remotes-config-dir.js b/tests/test-remotes-config-dir.js
index 9de8f01a..11d77348 100755
--- a/tests/test-remotes-config-dir.js
+++ b/tests/test-remotes-config-dir.js
@@ -32,7 +32,7 @@ function assertNotEquals(a, b) {
 	throw new Error("assertion failed " + JSON.stringify(a) + " != " + JSON.stringify(b));
 }
 
-print('1..3')
+print('1..4')
 
 let remotesDir = Gio.File.new_for_path('remotes.d');
 remotesDir.make_directory(null);
@@ -56,7 +56,8 @@ assertNotEquals(remotes.indexOf('foo'), -1);
 
 print("ok read-remotes-config-dir");
 
-// Adding a remote should not go in the remotes.d dir
+// Adding a remote should not go in the remotes.d dir unless this is a
+// system repo or add-remotes-config-dir is set to true
 repo.remote_add('bar', 'http://bar', null, null);
 remotes = repo.remote_list()
 assertNotEquals(remotes.indexOf('bar'), -1);
@@ -71,3 +72,16 @@ assertEquals(remotes.indexOf('foo'), -1);
 assertEquals(remotesDir.get_child('foo.conf').query_exists(null), false);
 
 print("ok delete-in-remotes-config-dir");
+
+// Set add-remotes-config-dir to true and check that a remote gets added
+// in the config dir
+let repoConfig = repo.copy_config();
+repoConfig.set_boolean('core', 'add-remotes-config-dir', true);
+repo.write_config(repoConfig);
+repo.reload_config(null);
+repo.remote_add('baz', 'http://baz', null, null);
+remotes = repo.remote_list()
+assertNotEquals(remotes.indexOf('baz'), -1);
+assertEquals(remotesDir.get_child('baz.conf').query_exists(null), true);
+
+print("ok add-in-remotes-config-dir");