diff --git a/nixos/modules/module-list.nix b/nixos/modules/module-list.nix
index 2bcf6e8dee31..4e0bff076794 100644
--- a/nixos/modules/module-list.nix
+++ b/nixos/modules/module-list.nix
@@ -226,7 +226,7 @@
   ./programs/zsh/zsh-autosuggestions.nix
   ./programs/zsh/zsh-syntax-highlighting.nix
   ./rename.nix
-  ./security/acme.nix
+  ./security/acme
   ./security/apparmor.nix
   ./security/audit.nix
   ./security/auditd.nix
diff --git a/nixos/modules/security/acme.nix b/nixos/modules/security/acme/default.nix
similarity index 99%
rename from nixos/modules/security/acme.nix
rename to nixos/modules/security/acme/default.nix
index e244989d6408..d827c448055b 100644
--- a/nixos/modules/security/acme.nix
+++ b/nixos/modules/security/acme/default.nix
@@ -916,6 +916,6 @@ in {
 
   meta = {
     maintainers = lib.teams.acme.members;
-    doc = ./acme.xml;
+    doc = ./doc.xml;
   };
 }
diff --git a/nixos/modules/security/acme.xml b/nixos/modules/security/acme/doc.xml
similarity index 100%
rename from nixos/modules/security/acme.xml
rename to nixos/modules/security/acme/doc.xml
diff --git a/nixos/modules/security/acme/mk-cert-ownership-assertion.nix b/nixos/modules/security/acme/mk-cert-ownership-assertion.nix
new file mode 100644
index 000000000000..b80d89aeb9fc
--- /dev/null
+++ b/nixos/modules/security/acme/mk-cert-ownership-assertion.nix
@@ -0,0 +1,4 @@
+{ cert, group, groups, user }: {
+  assertion = cert.group == group || builtins.any (u: u == user) groups.${cert.group}.members;
+  message = "Group for certificate ${cert.domain} must be ${group}, or user ${user} must be a member of group ${cert.group}";
+}
diff --git a/nixos/modules/services/web-servers/apache-httpd/default.nix b/nixos/modules/services/web-servers/apache-httpd/default.nix
index 1a49b4ca15c7..d817ff6019a3 100644
--- a/nixos/modules/services/web-servers/apache-httpd/default.nix
+++ b/nixos/modules/services/web-servers/apache-httpd/default.nix
@@ -370,6 +370,8 @@ let
       cat ${php.phpIni} > $out
       echo "$options" >> $out
     '';
+
+  mkCertOwnershipAssertion = import ../../../security/acme/mk-cert-ownership-assertion.nix;
 in
 
 
@@ -657,7 +659,11 @@ in
           `services.httpd.virtualHosts.<name>.useACMEHost` are mutually exclusive.
         '';
       }
-    ];
+    ] ++ map (name: mkCertOwnershipAssertion {
+      inherit (cfg) group user;
+      cert = config.security.acme.certs.${name};
+      groups = config.users.groups;
+    }) dependentCertNames;
 
     warnings =
       mapAttrsToList (name: hostOpts: ''
diff --git a/nixos/modules/services/web-servers/caddy/default.nix b/nixos/modules/services/web-servers/caddy/default.nix
index a4ada662cfbd..2b8c6f2e308b 100644
--- a/nixos/modules/services/web-servers/caddy/default.nix
+++ b/nixos/modules/services/web-servers/caddy/default.nix
@@ -38,6 +38,10 @@ let
       '';
     in
       if pkgs.stdenv.buildPlatform == pkgs.stdenv.hostPlatform then Caddyfile-formatted else Caddyfile;
+
+  acmeHosts = unique (catAttrs "useACMEHost" acmeVHosts);
+
+  mkCertOwnershipAssertion = import ../../../security/acme/mk-cert-ownership-assertion.nix;
 in
 {
   imports = [
@@ -266,7 +270,11 @@ in
       { assertion = cfg.adapter != "caddyfile" -> cfg.configFile != configFile;
         message = "Any value other than 'caddyfile' is only valid when providing your own `services.caddy.configFile`";
       }
-    ];
+    ] ++ map (name: mkCertOwnershipAssertion {
+      inherit (cfg) group user;
+      cert = config.security.acme.certs.${name};
+      groups = config.users.groups;
+    }) acmeHosts;
 
     services.caddy.extraConfig = concatMapStringsSep "\n" mkVHostConf virtualHosts;
     services.caddy.globalConfig = ''
@@ -323,8 +331,7 @@ in
 
     security.acme.certs =
       let
-        eachACMEHost = unique (catAttrs "useACMEHost" acmeVHosts);
-        reloads = map (useACMEHost: nameValuePair useACMEHost { reloadServices = [ "caddy.service" ]; }) eachACMEHost;
+        reloads = map (useACMEHost: nameValuePair useACMEHost { reloadServices = [ "caddy.service" ]; }) acmeHosts;
       in
         listToAttrs reloads;
 
diff --git a/nixos/modules/services/web-servers/nginx/default.nix b/nixos/modules/services/web-servers/nginx/default.nix
index dc174c8b41d0..41bce3669c58 100644
--- a/nixos/modules/services/web-servers/nginx/default.nix
+++ b/nixos/modules/services/web-servers/nginx/default.nix
@@ -374,6 +374,8 @@ let
       ${user}:{PLAIN}${password}
     '') authDef)
   );
+
+  mkCertOwnershipAssertion = import ../../../security/acme/mk-cert-ownership-assertion.nix;
 in
 
 {
@@ -842,7 +844,11 @@ in
           services.nginx.virtualHosts.<name>.useACMEHost are mutually exclusive.
         '';
       }
-    ];
+    ] ++ map (name: mkCertOwnershipAssertion {
+      inherit (cfg) group user;
+      cert = config.security.acme.certs.${name};
+      groups = config.users.groups;
+    }) dependentCertNames;
 
     systemd.services.nginx = {
       description = "Nginx Web Server";
diff --git a/nixos/tests/acme.nix b/nixos/tests/acme.nix
index 0dd7743c52b6..2dd06a50f40b 100644
--- a/nixos/tests/acme.nix
+++ b/nixos/tests/acme.nix
@@ -54,15 +54,15 @@ import ./make-test-python.nix ({ pkgs, lib, ... }: let
     baseConfig = { nodes, config, specialConfig ? {} }: lib.mkMerge [
       {
         security.acme = {
-          defaults = (dnsConfig nodes) // {
-            inherit group;
-          };
+          defaults = (dnsConfig nodes);
           # One manual wildcard cert
           certs."example.test" = {
             domain = "*.example.test";
           };
         };
 
+        users.users."${config.services."${server}".user}".extraGroups = ["acme"];
+
         services."${server}" = {
           enable = true;
           virtualHosts = {
@@ -252,15 +252,15 @@ in {
       } // (let
         baseCaddyConfig = { nodes, config, ... }: {
           security.acme = {
-            defaults = (dnsConfig nodes) // {
-              group = config.services.caddy.group;
-            };
+            defaults = (dnsConfig nodes);
             # One manual wildcard cert
             certs."example.test" = {
               domain = "*.example.test";
             };
           };
 
+          users.users."${config.services.caddy.user}".extraGroups = ["acme"];
+
           services.caddy = {
             enable = true;
             virtualHosts."a.exmaple.test" = {