diff --git a/debian/control b/debian/control
index 7158d342..1750c3c7 100644
--- a/debian/control
+++ b/debian/control
@@ -39,6 +39,7 @@ Multi-arch: no
 Depends:
  gir1.2-glib-2.0,
  mogwai-scheduled,
+ ostree,
  python3-gi,
  systemd (>= 200),
  ${misc:Depends},
diff --git a/debian/eos-updater.install b/debian/eos-updater.install
index fed07095..144e100c 100644
--- a/debian/eos-updater.install
+++ b/debian/eos-updater.install
@@ -2,12 +2,14 @@ lib/systemd/system/eos-autoupdater.service
 lib/systemd/system/eos-autoupdater.timer
 lib/systemd/system/eos-updater-avahi.path
 lib/systemd/system/eos-updater-avahi.service
+lib/systemd/system/eos-updater-autocleanup.service
 lib/systemd/system/eos-updater-flatpak-installer.service
 lib/systemd/system/eos-updater-flatpak-installer-fallback.service
 lib/systemd/system/eos-updater-flatpak-installer-fallback.timer
 lib/systemd/system/eos-updater.service
 lib/systemd/system/eos-update-server.service
 lib/systemd/system/eos-update-server.socket
+lib/systemd/system/ostree-finalize-staged.service.d/autocleanup.conf
 usr/libexec/eos-updater
 usr/libexec/eos-autoupdater
 usr/libexec/eos-updater-avahi
diff --git a/eos-updater/eos-updater-autocleanup.service.in b/eos-updater/eos-updater-autocleanup.service.in
new file mode 100644
index 00000000..0d20e2e4
--- /dev/null
+++ b/eos-updater/eos-updater-autocleanup.service.in
@@ -0,0 +1,37 @@
+[Unit]
+Description=Automatically cleanup after staged Endless OS Updater deployment
+Documentation=man:ostree-admin-cleanup(1) man:eos-updater(8)
+
+# Run ostree admin cleanup only if /sysroot/.cleanup is present and then
+# delete it when cleanup is successful.
+#
+# FIXME: Drop this when https://github.com/ostreedev/ostree/issues/2510
+# is resolved.
+ConditionPathExists=/sysroot/.cleanup
+
+# We want this to be triggered by multi-user.target but not block it via
+# the default After added to target units since pruning the repo can be
+# slow. See the Default Dependencies sections in systemd.service(5) and
+# systemd.target(5).
+DefaultDependencies=no
+Requires=sysinit.target
+After=sysinit.target basic.target
+Conflicts=shutdown.target
+Before=shutdown.target
+
+[Service]
+Type=oneshot
+RemainAfterExit=yes
+ExecStart=@ostree@ admin cleanup
+ExecStart=/bin/rm -f /sysroot/.cleanup
+
+# Only /sysroot and /boot need to be written to.
+ProtectSystem=strict
+ReadWritePaths=/sysroot /boot
+
+# This will be allowed to run in the background, so try to make it less
+# disruptive while it prunes the repo.
+IOSchedulingClass=idle
+
+[Install]
+WantedBy=multi-user.target
diff --git a/eos-updater/finalize-autocleanup.conf.in b/eos-updater/finalize-autocleanup.conf.in
new file mode 100644
index 00000000..f1804947
--- /dev/null
+++ b/eos-updater/finalize-autocleanup.conf.in
@@ -0,0 +1,9 @@
+# This is a drop-in file for ostree-finalize-staged.service.
+#
+# FIXME: Drop this when https://github.com/ostreedev/ostree/issues/2510
+# is resolved.
+
+[Service]
+# After finalizing the staged deployment, touch the .cleanup file so
+# that the cleanup can be completed on the next boot.
+ExecStop=-/bin/touch /sysroot/.cleanup
diff --git a/eos-updater/meson.build b/eos-updater/meson.build
index dd4d5a19..61156308 100644
--- a/eos-updater/meson.build
+++ b/eos-updater/meson.build
@@ -105,6 +105,7 @@ install_data(
 # systemd files
 config = configuration_data()
 config.set('libexecdir', join_paths(get_option('prefix'), get_option('libexecdir')))
+config.set('ostree', find_program('ostree').path())
 
 configure_file(
   input: 'eos-updater.service.in',
@@ -113,6 +114,20 @@ configure_file(
   configuration: config,
 )
 
+configure_file(
+  input: 'eos-updater-autocleanup.service.in',
+  output: 'eos-updater-autocleanup.service',
+  install_dir: dependency('systemd').get_pkgconfig_variable('systemdsystemunitdir'),
+  configuration: config,
+)
+
+configure_file(
+  input: 'finalize-autocleanup.conf.in',
+  output: 'autocleanup.conf',
+  install_dir: join_paths(dependency('systemd').get_pkgconfig_variable('systemdsystemunitdir'), 'ostree-finalize-staged.service.d'),
+  configuration: config,
+)
+
 # Example configuration
 install_data(
   files('eos-updater.conf'),