diff --git a/salt/manager/sync_es_users.sls b/salt/manager/sync_es_users.sls
index 29b090e18..8fc9c6bb4 100644
--- a/salt/manager/sync_es_users.sls
+++ b/salt/manager/sync_es_users.sls
@@ -31,11 +31,13 @@ sync_es_users:
       - http: wait_for_kratos
       - file: so-user.lock # require so-user.lock file to be missing
 
-# we dont want this added too early in setup, so we add the onlyif to verify 'startup_states: highstate'
-# is in the minion config. That line is added before the final highstate during setup
+# we dont want this added too early in setup, so the onlyif gates on the
+# /opt/so/state/setup-complete marker. The marker is written by
+# mark_setup_complete in setup/so-functions just before the final setup
+# highstate (and by an upgrade-path state for systems set up under the old gate).
 so-user_sync:
   cron.present:
     - user: root
     - name: 'PATH=/usr/local/sbin:/usr/local/bin:/sbin:/bin:/usr/sbin:/usr/bin:/root/bin /usr/sbin/so-user sync &>> /opt/so/log/soc/sync.log'
     - identifier: so-user_sync
-    - onlyif: "grep -x 'startup_states: highstate' /etc/salt/minion"
+    - onlyif: "test -e /opt/so/state/setup-complete"
diff --git a/salt/salt/minion/boot_highstate.sls b/salt/salt/minion/boot_highstate.sls
new file mode 100644
index 000000000..eb2596dad
--- /dev/null
+++ b/salt/salt/minion/boot_highstate.sls
@@ -0,0 +1,31 @@
+# Copyright Security Onion Solutions LLC and/or licensed to Security Onion Solutions LLC under one
+# or more contributor license agreements. Licensed under the Elastic License 2.0 as shown at
+# https://securityonion.net/license; you may not use this file except in compliance with the
+# Elastic License 2.0.
+
+# Manages /etc/systemd/system/so-boot-highstate.service, a Type=oneshot
+# RemainAfterExit=yes unit that runs `salt-call state.highstate` exactly once
+# per system boot. Replaces the legacy `startup_states: highstate` minion
+# config, which fired on every salt-minion service restart (causing a redundant
+# highstate whenever a highstate itself restarted salt-minion).
+
+include:
+  - systemd.reload
+
+so_boot_highstate_unit_file:
+  file.managed:
+    - name: /etc/systemd/system/so-boot-highstate.service
+    - source: salt://salt/service/so-boot-highstate.service
+    - onchanges_in:
+      - module: systemd_reload
+
+# Only enable once setup is complete. Until then the gate file is missing and
+# the unit's own ConditionPathExists would no-op it anyway -- this just keeps
+# `systemctl is-enabled` honest for the sync_es_users gate.
+so_boot_highstate_service:
+  service.enabled:
+    - name: so-boot-highstate.service
+    - onlyif: test -e /opt/so/state/setup-complete
+    - require:
+      - file: so_boot_highstate_unit_file
+      - module: systemd_reload
diff --git a/salt/salt/minion/init.sls b/salt/salt/minion/init.sls
index eb7018aed..59dd0289c 100644
--- a/salt/salt/minion/init.sls
+++ b/salt/salt/minion/init.sls
@@ -17,6 +17,7 @@ include:
   - repo.client
   - salt.mine_functions
   - salt.minion.service_file
+  - salt.minion.boot_highstate
 {% if GLOBALS.is_manager %}
   - ca.signing_policy
 {% endif %}
@@ -80,11 +81,33 @@ set_log_levels:
       - "log_level: info"
       - "log_level_logfile: info"
 
-enable_startup_states:
-  file.uncomment:
+# startup_states: highstate caused a full highstate to run on every
+# salt-minion service start, including the restart triggered when a highstate
+# itself modified the minion config (beacons, mine, unit file). Replaced by
+# so-boot-highstate.service (managed in salt.minion.boot_highstate), which
+# runs once per system boot only. Strip the line from /etc/salt/minion on
+# upgrade; both the commented and uncommented forms historically existed.
+remove_startup_states:
+  file.line:
     - name: /etc/salt/minion
-    - regex: '^startup_states: highstate$'
-    - unless: pgrep so-setup
+    - match: 'startup_states: highstate'
+    - mode: delete
+
+# Upgrade-path bridge: systems that already passed setup under the old gate
+# (`grep -x 'startup_states: highstate' /etc/salt/minion`) get a /opt/so/state/setup-complete
+# marker so so-boot-highstate.service can be enabled and the so-user_sync cron
+# in sync_es_users.sls keeps installing. Setup-in-progress systems instead get
+# the marker from `mark_setup_complete` in setup/so-functions at the right
+# moment. `replace: false` means we never overwrite a marker once written.
+mark_setup_complete_for_upgrades:
+  file.managed:
+    - name: /opt/so/state/setup-complete
+    - replace: false
+    - makedirs: True
+    - onlyif: "grep -qx 'startup_states: highstate' /etc/salt/minion"
+    - require_in:
+      - file: remove_startup_states
+      - service: so_boot_highstate_service
 
 {% endif %}
 
diff --git a/salt/salt/service/so-boot-highstate.service b/salt/salt/service/so-boot-highstate.service
new file mode 100644
index 000000000..cc8c6a1c6
--- /dev/null
+++ b/salt/salt/service/so-boot-highstate.service
@@ -0,0 +1,14 @@
+[Unit]
+Description=Security Onion boot-time highstate (runs once per boot)
+After=salt-minion.service network-online.target docker.service
+Wants=network-online.target docker.service
+Requires=salt-minion.service
+ConditionPathExists=/opt/so/state/setup-complete
+
+[Service]
+Type=oneshot
+RemainAfterExit=yes
+ExecStart=/usr/bin/salt-call state.highstate -l info queue=True
+
+[Install]
+WantedBy=multi-user.target
diff --git a/salt/setup/virt/setSalt.sls b/salt/setup/virt/setSalt.sls
index 69c8795de..59ab9e1e3 100644
--- a/salt/setup/virt/setSalt.sls
+++ b/salt/setup/virt/setSalt.sls
@@ -8,11 +8,6 @@ set_role_grain:
     - name: role
     - value: so-{{ grains.id.split("_") | last }}
 
-set_highstate:
-  file.append:
-    - name: /etc/salt/minion
-    - text: 'startup_states: highstate'
-
 enable_salt_minion:
   service.enabled:
     - name: salt-minion
diff --git a/setup/so-functions b/setup/so-functions
index c94b8eee7..5ce9a8fdc 100755
--- a/setup/so-functions
+++ b/setup/so-functions
@@ -539,16 +539,19 @@ configure_minion() {
 		"  x509_v2: true"\
 		"log_level: info"\
 		"log_level_logfile: info"\
-		"log_file: /opt/so/log/salt/minion"\
-		"#startup_states: highstate" >> "$minion_config"
+		"log_file: /opt/so/log/salt/minion" >> "$minion_config"
 
 }
 
-checkin_at_boot() {
-	local minion_config=/etc/salt/minion
+mark_setup_complete() {
+	# Writes the setup-complete marker. Salt's so-boot-highstate.service
+	# (boot-time oneshot) and the so-user_sync cron gate in
+	# salt/manager/sync_es_users.sls both key off this file.
+	local marker=/opt/so/state/setup-complete
 
-	info "Enabling checkin at boot"
-	sed -i 's/#startup_states: highstate/startup_states: highstate/' "$minion_config"
+	info "Marking setup as complete"
+	mkdir -p "$(dirname "$marker")"
+	touch "$marker"
 }
 
 check_requirements() {
diff --git a/setup/so-setup b/setup/so-setup
index 6c77e781c..c11d287eb 100755
--- a/setup/so-setup
+++ b/setup/so-setup
@@ -792,7 +792,7 @@ if ! [[ -f $install_opt_file ]]; then
 			error "Failed to run so-elastic-fleet-setup"
 			fail_setup
 		fi
-		checkin_at_boot
+		mark_setup_complete
 		set_initial_firewall_access
         initialize_elasticsearch_indices "so-case so-casehistory so-assistant-session so-assistant-chat"
 		# run a final highstate before enabling scheduled highstates.