diff --git a/locales/en.json b/locales/en.json
index 8aeafb936..46d2f03b8 100644
--- a/locales/en.json
+++ b/locales/en.json
@@ -593,6 +593,7 @@
     "migration_0024_rebuild_python_venv_in_progress": "Now attempting to rebuild the Python virtualenv for `{app}`",
     "migration_description_0027_migrate_to_bookworm": "Upgrade the system to Debian Bookworm and YunoHost 12",
     "migration_0027_cleaning_up": "Cleaning up cache and packages not useful anymore…",
+    "migration_0027_delayed_api_restart": "The YunoHost API will automatically be restarted in 15 seconds. It may be unavailable for a few seconds, and then you will have to login again.",
     "migration_0027_general_warning": "Please note that this migration is a delicate operation. The YunoHost team did its best to review and test it, but the migration might still break parts of the system or its apps.\n\nTherefore, it is recommended to:\n    - Perform a backup of any critical data or app. More info on https://yunohost.org/backup;\n    - Be patient after launching the migration: Depending on your Internet connection and hardware, it might take up to a few hours for everything to upgrade.",
     "migration_0027_main_upgrade": "Starting main upgrade…",
     "migration_0027_modified_files": "Please note that the following files were found to be manually modified and might be overwritten following the upgrade: {manually_modified_files}",
@@ -796,4 +797,4 @@
     "yunohost_installing": "Installing YunoHost…",
     "yunohost_not_installed": "YunoHost is not correctly installed. Please run 'yunohost tools postinstall'",
     "yunohost_postinstall_end_tip": "The post-install completed! To finalize your setup, please consider:\n    - diagnose potential issues through the 'Diagnosis' section of the webadmin (or 'yunohost diagnosis run' in command-line);\n    - reading the 'Finalizing your setup' and 'Getting to know YunoHost' parts in the admin documentation: https://yunohost.org/admindoc."
-}
\ No newline at end of file
+}
diff --git a/src/migrations/0027_migrate_to_bookworm.py b/src/migrations/0027_migrate_to_bookworm.py
index 9ff497398..e3d6007c6 100644
--- a/src/migrations/0027_migrate_to_bookworm.py
+++ b/src/migrations/0027_migrate_to_bookworm.py
@@ -1,5 +1,6 @@
 import glob
 import os
+import subprocess
 
 from moulinette import m18n
 from yunohost.utils.error import YunohostError
@@ -230,6 +231,16 @@ class MyMigration(Migration):
         #postupgradecmds += "echo 'Restarting nginx...' >&2\n"
         #postupgradecmds += "systemctl restart nginx\n"
 
+        # If running from the webadmin, restart the API after a delay
+        if Moulinette.interface.type == "api":
+            logger.warning(m18n.n("migration_0027_delayed_api_restart"))
+            sleep(5)
+            # Restart the API after 10 sec (at now doesn't support sub-minute times...)
+            # We do this so that the API / webadmin still gets the proper HTTP response
+            cmd = 'at -M now >/dev/null 2>&1 <<< "sleep 10; systemctl restart yunohost-api"'
+            # For some reason subprocess doesn't like the redirections so we have to use bash -c explicity...
+            subprocess.check_call(["bash", "-c", cmd])
+
     def debian_major_version(self):
         # The python module "platform" and lsb_release are not reliable because
         # on some setup, they may still return Release=9 even after upgrading to
diff --git a/src/utils/system.py b/src/utils/system.py
index 105aea704..690c8f3c8 100644
--- a/src/utils/system.py
+++ b/src/utils/system.py
@@ -287,6 +287,11 @@ def aptitude_with_progress_bar(cmd):
         f'LC_ALL=C DEBIAN_FRONTEND=noninteractive APT_LISTCHANGES_FRONTEND=none aptitude {cmd} --quiet=2 -o=Dpkg::Use-Pty=0 -o "APT::Status-Fd=$YNH_STDINFO"'
     )
 
+    # If upgrading yunohost from the API, delay the Yunohost-api restart
+    # (this should be the last time we need it before bookworm, because on bookworm, yunohost-admin cookies will be persistent upon api restart)
+    if " yunohost " in cmd and Moulinette.interface.type == "api":
+        cmd = "YUNOHOST_API_RESTART_WILL_BE_HANDLED_BY_YUNOHOST=yes " + cmd
+
     logger.debug(f"Running: {cmd}")
 
     ret = call_async_output(cmd, callbacks, shell=True)