diff --git a/install/share/Makefile.am b/install/share/Makefile.am
index 684da8dde..6c4c3f0ed 100644
--- a/install/share/Makefile.am
+++ b/install/share/Makefile.am
@@ -106,6 +106,7 @@ dist_app_DATA =				\
 	pki-acme-database.conf.template	\
 	pki-acme-engine.conf.template	\
 	pki-acme-issuer.conf.template	\
+	pki-acme-realm.conf.template	\
 	ldbm-tuning.ldif		\
 	$(NULL)
 
diff --git a/install/share/pki-acme-engine.conf.template b/install/share/pki-acme-engine.conf.template
index cb9898c5f..e6a56593f 100644
--- a/install/share/pki-acme-engine.conf.template
+++ b/install/share/pki-acme-engine.conf.template
@@ -1,2 +1,11 @@
+# Parameters read by ACMEEngineConfigFileSource, i.e. these are
+# expected to be in the file pointed to by the 'filename' directive
+# above.
+#
+# IPA only sets the values it uses.
+#
+# Whether to enable the ACME service:
 enabled=false
-wildcard=false
+
+# Whether to accept wildcard DNS identifiers:
+policy.wildcard=false
diff --git a/install/share/pki-acme-issuer.conf.template b/install/share/pki-acme-issuer.conf.template
index de2a06fec..968d08f0a 100644
--- a/install/share/pki-acme-issuer.conf.template
+++ b/install/share/pki-acme-issuer.conf.template
@@ -1,5 +1,5 @@
 class=org.dogtagpki.acme.issuer.PKIIssuer
 url=https://$FQDN:8443
-profile=acmeServerCert
+profile=acmeIPAServerCert
 username=$USER
 password=$PASSWORD
diff --git a/install/share/pki-acme-realm.conf.template b/install/share/pki-acme-realm.conf.template
new file mode 100644
index 000000000..2e9c1607b
--- /dev/null
+++ b/install/share/pki-acme-realm.conf.template
@@ -0,0 +1,8 @@
+authType=BasicAuth
+class=org.dogtagpki.acme.realm.DSRealm
+groupsDN=ou=groups,o=ipaca
+usersDN=ou=people,o=ipaca
+url=ldaps://$FQDN:636
+configFile=/etc/pki/pki-tomcat/ca/CS.cfg
+username=$USER
+password=$PASSWORD
diff --git a/install/share/profiles/Makefile.am b/install/share/profiles/Makefile.am
index eb53703cc..a04902cce 100644
--- a/install/share/profiles/Makefile.am
+++ b/install/share/profiles/Makefile.am
@@ -7,7 +7,7 @@ app_DATA =				\
 	caIPAserviceCert.UPGRADE.cfg	\
 	IECUserRoles.cfg		\
 	KDCs_PKINIT_Certs.cfg		\
-	acmeServerCert.cfg		\
+	acmeIPAServerCert.cfg		\
 	$(NULL)
 
 EXTRA_DIST =				\
diff --git a/install/share/profiles/acmeIPAServerCert.cfg b/install/share/profiles/acmeIPAServerCert.cfg
index e636e29ed..2487056e1 100644
--- a/install/share/profiles/acmeIPAServerCert.cfg
+++ b/install/share/profiles/acmeIPAServerCert.cfg
@@ -1,4 +1,4 @@
-profileId=acmeServerCert
+profileId=acmeIPAServerCert
 classId=caEnrollImpl
 desc=ACME profile for use in IPA deployments
 visible=true
diff --git a/ipaplatform/base/paths.py b/ipaplatform/base/paths.py
index 234f66a35..b46e661ad 100644
--- a/ipaplatform/base/paths.py
+++ b/ipaplatform/base/paths.py
@@ -127,6 +127,7 @@ class BasePathNamespace:
     PKI_ACME_DATABASE_CONF = "/etc/pki/pki-tomcat/acme/database.conf"
     PKI_ACME_ENGINE_CONF = "/etc/pki/pki-tomcat/acme/engine.conf"
     PKI_ACME_ISSUER_CONF = "/etc/pki/pki-tomcat/acme/issuer.conf"
+    PKI_ACME_REALM_CONF = "/etc/pki/pki-tomcat/acme/realm.conf"
     ETC_REDHAT_RELEASE = "/etc/redhat-release"
     RESOLV_CONF = "/etc/resolv.conf"
     SAMBA_KEYTAB = "/etc/samba/samba.keytab"
diff --git a/ipapython/dogtag.py b/ipapython/dogtag.py
index abd96bd45..251281a7e 100644
--- a/ipapython/dogtag.py
+++ b/ipapython/dogtag.py
@@ -56,8 +56,8 @@ INCLUDED_PROFILES = {
     Profile(u'KDCs_PKINIT_Certs',
             u'Profile for PKINIT support by KDCs',
             False),
-    Profile(u'acmeServerCert',
-            u'ACME service certificate profile',
+    Profile(u'acmeIPAServerCert',
+            u'ACME IPA service certificate profile',
             False),
     }
 
diff --git a/ipaserver/install/cainstance.py b/ipaserver/install/cainstance.py
index fca829de0..6c84e928b 100644
--- a/ipaserver/install/cainstance.py
+++ b/ipaserver/install/cainstance.py
@@ -71,7 +71,7 @@ ADMIN_GROUPS = [
     'Security Domain Administrators'
 ]
 
-ACME_AGENT_GROUP = 'ACME Agents'
+ACME_AGENT_GROUP = 'Enterprise ACME Administrators'
 
 PROFILES_DN = DN(('ou', 'certificateProfiles'), ('ou', 'ca'), ('o', 'ipaca'))
 
@@ -768,6 +768,12 @@ class CAInstance(DogtagInstance):
             self.basedn)
         conn.add_entry_to_group(user_dn, group_dn, 'uniqueMember')
 
+        group_dn = DN(('cn', ACME_AGENT_GROUP), ('ou', 'groups'),
+                      self.basedn)
+        conn.add_entry_to_group(user_dn, group_dn, 'uniqueMember')
+
+        conn.disconnect()
+
     def __get_ca_chain(self):
         try:
             return dogtag.get_ca_certchain(ca_host=self.fqdn)
@@ -1479,6 +1485,8 @@ class CAInstance(DogtagInstance):
             logger.debug('ACME service is already deployed')
             return False
 
+        self._ldap_mod('/usr/share/pki/acme/database/ds/schema.ldif')
+
         configure_acme_acls()
 
         # create ACME agent group (if not exist already) and user
@@ -1510,6 +1518,7 @@ class CAInstance(DogtagInstance):
             ('pki-acme-database.conf.template', paths.PKI_ACME_DATABASE_CONF),
             ('pki-acme-engine.conf.template', paths.PKI_ACME_ENGINE_CONF),
             ('pki-acme-issuer.conf.template', paths.PKI_ACME_ISSUER_CONF),
+            ('pki-acme-realm.conf.template', paths.PKI_ACME_REALM_CONF),
         ]
         sub_dict = dict(
             FQDN=self.fqdn,
@@ -1732,6 +1741,11 @@ def ensure_acme_containers():
         DN(('ou', 'orders'), ou_acme),
         DN(('ou', 'authorizations'), ou_acme),
         DN(('ou', 'challenges'), ou_acme),
+        DN(('ou', 'certificates'), ou_acme),
+    ]
+
+    extensible_rdns = [
+        DN(('ou', 'config'), ou_acme),
     ]
 
     for rdn in rdns:
@@ -1741,6 +1755,13 @@ def ensure_acme_containers():
             ou=[rdn[0][0].value],
         )
 
+    for rdn in extensible_rdns:
+        ensure_entry(
+            DN(rdn, ('o', 'ipaca')),
+            objectclass=['top', 'organizationalUnit', 'extensibleObject'],
+            ou=[rdn[0][0].value],
+        )
+
 
 def ensure_entry(dn, **attrs):
     """Ensure an entry exists.
diff --git a/ipaserver/install/ipa_acme_manage.py b/ipaserver/install/ipa_acme_manage.py
index ff56d3bf6..d3dcb135a 100644
--- a/ipaserver/install/ipa_acme_manage.py
+++ b/ipaserver/install/ipa_acme_manage.py
@@ -3,13 +3,16 @@
 #
 
 import enum
-import pathlib
 
+from ipalib import api, errors
+from ipalib import _
+from ipalib.facts import is_ipa_configured
 from ipaplatform.paths import paths
 from ipapython.admintool import AdminTool
-from ipapython.directivesetter import DirectiveSetter
+from ipapython import cookie, dogtag
 from ipaserver.install import cainstance
-from ipalib.facts import is_ipa_configured
+
+from ipaserver.plugins.dogtag import RestClient
 
 # Manages the FreeIPA ACME service on a per-server basis.
 #
@@ -20,6 +23,49 @@ from ipalib.facts import is_ipa_configured
 # remove this program, or make it a wrapper for the API commands.
 
 
+class acme_state(RestClient):
+
+    def _request(self, url):
+        return dogtag.https_request(
+            self.ca_host, 8443,
+            url=url,
+            cafile=self.ca_cert,
+            client_certfile=paths.RA_AGENT_PEM,
+            client_keyfile=paths.RA_AGENT_KEY,
+            method='POST'
+        )
+
+    def __enter__(self):
+        status, resp_headers, _unused = self._request('/acme/login')
+        cookies = cookie.Cookie.parse(resp_headers.get('set-cookie', ''))
+        if status != 200 or len(cookies) == 0:
+            raise errors.RemoteRetrieveError(
+                reason=_('Failed to authenticate to CA REST API')
+            )
+        object.__setattr__(self, 'cookie', str(cookies[0]))
+        return self
+
+    def __exit__(self, exc_type, exc_value, traceback):
+        """Log out of the REST API"""
+        headers = dict(Cookie=self.cookie)
+        status, unused, _unused = self._request('/acme/logout')
+        object.__setattr__(self, 'cookie', None)
+        if status != 204:
+            raise RuntimeError('Failed to logout')
+
+    def enable(self):
+        headers = dict(Cookie=self.cookie)
+        status, unused, _unused = self._request('/acme/enable')
+        if status != 200:
+            raise RuntimeError('Failed to enable ACME')
+
+    def disable(self):
+        headers = dict(Cookie=self.cookie)
+        status, unused, _unused = self._request('/acme/disable')
+        if status != 200:
+            raise RuntimeError('Failed to disble ACME')
+
+
 class Command(enum.Enum):
     ENABLE = 'enable'
     DISABLE = 'disable'
@@ -52,28 +98,17 @@ class IPAACMEManage(AdminTool):
             print("CA is not installed on this server.")
             return 1
 
-        if self.command == Command.ENABLE:
-            directive = 'enabled'
-            value = 'true'
-        elif self.command == Command.DISABLE:
-            directive = 'enabled'
-            value = 'false'
-        else:
-            raise RuntimeError('programmer error: unhandled enum case')
+        api.bootstrap(in_server=True, confdir=paths.ETC_IPA)
+        api.finalize()
+        api.Backend.ldap2.connect()
 
-        with DirectiveSetter(
-            paths.PKI_ACME_ENGINE_CONF,
-            separator='=',
-            quotes=False,
-        ) as ds:
-            ds.set(directive, value)
-
-        # Work around a limitation in PKI ACME service file watching
-        # where renames (what DirectiveSetter does) are not detected.
-        # It will be fixed, but keeping the workaround will do no harm.
-        pathlib.Path(paths.PKI_ACME_ENGINE_CONF).touch()
-
-        # Nothing else to do; the Dogtag ACME service monitors engine.conf
-        # for updates and reconfigures itself as required.
+        state = acme_state(api)
+        with state as ca_api:
+            if self.command == Command.ENABLE:
+                ca_api.enable()
+            elif self.command == Command.DISABLE:
+                ca_api.disable()
+            else:
+                raise RuntimeError('programmer error: unhandled enum case')
 
         return 0
diff --git a/ipaserver/install/server/upgrade.py b/ipaserver/install/server/upgrade.py
index ef58fd24c..18891d53c 100644
--- a/ipaserver/install/server/upgrade.py
+++ b/ipaserver/install/server/upgrade.py
@@ -1112,7 +1112,9 @@ def ca_upgrade_schema(ca):
         return False
 
     # ACME schema file moved in pki-server-10.9.0-0.3
+    # ACME database connections were abstrated in pki-acme-10.10.0
     for path in [
+        '/usr/share/pki/acme/conf/database/ds/schema.ldif',
         '/usr/share/pki/acme/conf/database/ldap/schema.ldif',
         '/usr/share/pki/acme/database/ldap/schema.ldif',
     ]: