diff --git a/src/etc/inc/plugins.inc.d/unbound.inc b/src/etc/inc/plugins.inc.d/unbound.inc
index 56f1fabdb..94d881784 100644
--- a/src/etc/inc/plugins.inc.d/unbound.inc
+++ b/src/etc/inc/plugins.inc.d/unbound.inc
@@ -259,19 +259,7 @@ EOF;
     $forward_local = '';
     $resolv_conf_root = '';
     if (isset($config['unbound']['forwarding'])) {
-        $dnsservers = array();
-
-        if (isset($config['system']['dnsallowoverride'])) {
-            foreach (get_nameservers() as $nameserver) {
-                $dnsservers[] = $nameserver;
-            }
-        }
-
-        if (!empty($config['system']['dnsserver'][0])) {
-            foreach ($config['system']['dnsserver'] as $nameserver) {
-                $dnsservers[] = $nameserver;
-            }
-        }
+        $dnsservers = get_nameservers();
 
         if (!empty($dnsservers)) {
             $forward_conf .= <<<EOD
diff --git a/src/etc/inc/system.inc b/src/etc/inc/system.inc
index 5030b9287..2da579cad 100644
--- a/src/etc/inc/system.inc
+++ b/src/etc/inc/system.inc
@@ -201,15 +201,14 @@ function system_resolvconf_generate($verbose = false)
 
     if (isset($syscfg['dnsallowoverride'])) {
         $search = array_merge($search, get_searchdomains());
-        foreach (get_nameservers(null, true) as $nameserver) {
-            $resolvconf .= "nameserver {$nameserver['host']}\n";
-            $routes[] = $nameserver;
-        }
     }
 
-    if (isset($syscfg['dnsserver'][0])) {
-        foreach ($syscfg['dnsserver'] as $ns) {
-            $resolvconf .= "nameserver $ns\n";
+    foreach (get_nameservers(null, true) as $dnsserver) {
+        $host = !empty($dnsserver['host']) ? $dnsserver['host'] : $dnsserver;
+        $resolvconf .= "nameserver {$host}\n";
+
+        if (!empty($dnsserver['gateway'])) {
+            $routes[] = $dnsserver;
         }
     }
 
@@ -235,16 +234,6 @@ function system_resolvconf_generate($verbose = false)
 
     rename($tempfile, '/etc/resolv.conf');
 
-    for ($dnscounter = 1; $dnscounter < 9; $dnscounter++) {
-        $dnsgw = "dns{$dnscounter}gw";
-        if (!empty($syscfg[$dnsgw])) {
-            $gwname = $syscfg[$dnsgw];
-            if ($gwname != 'none') {
-                $routes[] = ['host' => $syscfg['dnsserver'][$dnscounter - 1], 'gateway' => $gateways->getAddress($gwname)];
-            }
-        }
-    }
-
     /* XXX check for overlapping host routes */
 
     /* setup static routes for DNS servers as configured */
@@ -340,8 +329,32 @@ function get_nameservers($interface = null, $with_gateway = false)
     $master_list = array();
 
     $dns_lists = glob('/tmp/*_nameserver*');
+    $dns_static = [];
     $exclude_interfaces = [];
 
+    $gateways = new \OPNsense\Routing\Gateways(legacy_interfaces_details());
+
+    $syscfg = config_read_array('system');
+
+    for ($dnscounter = 1; $dnscounter < 9; $dnscounter++) {
+        $dnsgw = "dns{$dnscounter}gw";
+        if (!empty($syscfg[$dnsgw])) {
+            $gwname = $syscfg[$dnsgw];
+            $entry = $syscfg['dnsserver'][$dnscounter - 1];
+            if ($gwname != 'none') {
+                $dns_static[] = [
+                    'host' => $entry,
+                    'gw_addr' => $gateways->getAddress($gwname),
+                    'if' => $gateways->getInterface($gwname)
+                ];
+            } else if (!empty($entry)) {
+                $dns_static[] = $entry;
+            }
+        }
+    }
+
+    $dns_static_new = $dns_static;
+
     if (!empty($interface)) {
         /* only acquire servers provided for this interface */
         $realif = get_real_interface($interface);
@@ -350,8 +363,18 @@ function get_nameservers($interface = null, $with_gateway = false)
             "/tmp/{$realif}_nameserver",
             "/tmp/{$realifv6}_nameserverv6",
         ];
+
+        /* this interface can also be assigned multiple manual dns servers */
+        $dns_static_new = [];
+        foreach ($dns_static as $static) {
+            if (isset($static['if']) && $static['if'] == $realif) {
+                $dns_static_new[] = $static;
+            }
+        }
     }
 
+    $dns_static = $dns_static_new;
+
     if (isset($config['system']['dnsallowoverride_exclude'])) {
         foreach (explode(',', $config['system']['dnsallowoverride_exclude']) as $intf) {
             if (isset($config['interfaces'][$intf])) {
@@ -362,6 +385,10 @@ function get_nameservers($interface = null, $with_gateway = false)
     }
 
     foreach ($dns_lists as $fdns) {
+        if (!isset($syscfg['dnsallowoverride'])) {
+            continue;
+        }
+
         $intf = explode('_', basename($fdns))[0];
         if (in_array($intf, $exclude_interfaces)) {
             continue;
@@ -381,7 +408,7 @@ function get_nameservers($interface = null, $with_gateway = false)
         foreach ($contents as $dns) {
             if (!empty($dns) && is_ipaddr($dns)) {
                 if ($with_gateway) {
-                    $master_list[] = ['host' => $dns, 'gateway' => $gw];
+                    $master_list[] = ['type' => 'dynamic', 'host' => $dns, 'gateway' => $gw];
                 } else {
                     $master_list[] = $dns;
                 }
@@ -389,6 +416,18 @@ function get_nameservers($interface = null, $with_gateway = false)
         }
     }
 
+    foreach ($dns_static as $static) {
+        if (isset($static['if']) && in_array($static['if'], $exclude_interfaces)) {
+            continue;
+        }
+
+        if ($with_gateway && isset($static['gw_addr'])) {
+            $master_list[] = ['type' => 'static', 'host' => $static['host'], 'gateway' => $static['gw_addr']];
+        } else {
+            $master_list[] = isset($static['host']) ? $static['host'] : $static;
+        }
+    }
+
     return array_unique($master_list, SORT_REGULAR);
 }
 
diff --git a/src/opnsense/mvc/app/controllers/OPNsense/Unbound/Api/SettingsController.php b/src/opnsense/mvc/app/controllers/OPNsense/Unbound/Api/SettingsController.php
index 825d946e6..3051f7939 100644
--- a/src/opnsense/mvc/app/controllers/OPNsense/Unbound/Api/SettingsController.php
+++ b/src/opnsense/mvc/app/controllers/OPNsense/Unbound/Api/SettingsController.php
@@ -78,18 +78,7 @@ class SettingsController extends ApiMutableModelControllerBase
             $nameservers = json_decode(trim($backend->configdRun("system list nameservers")));
 
             if ($nameservers !== null) {
-                $result = array();
-                $config = Config::getInstance()->object();
-                if (isset($config->system->dnsallowoverride)) {
-                    foreach ($nameservers->dynamic as $dynamic) {
-                        $result[] = $dynamic;
-                    }
-                }
-                foreach ($nameservers->static as $static) {
-                    $result[] = $static;
-                }
-
-                return $result;
+                return $nameservers;
             }
         }
         return array("message" => "Unable to run configd action");
diff --git a/src/opnsense/scripts/system/nameservers.php b/src/opnsense/scripts/system/nameservers.php
index 48bb61626..73d26e779 100755
--- a/src/opnsense/scripts/system/nameservers.php
+++ b/src/opnsense/scripts/system/nameservers.php
@@ -30,23 +30,8 @@
 require_once 'config.inc';
 require_once 'system.inc';
 require_once 'util.inc';
+require_once 'interfaces.inc';
 
-use OPNsense\Core\Config;
-
-$config = Config::getInstance()->object();
-
-$result = array();
-
-/* get dynamic nameservers */
-foreach (get_nameservers() as $nameserver) {
-    $result["dynamic"][] = $nameserver;
-}
-
-/* get manually entered nameservers */
-foreach ($config->system->children() as $key => $node) {
-    if ($key == "dnsserver") {
-        $result["static"][] = (string)$node;
-    }
-}
+$result = get_nameservers();
 
 echo json_encode($result) . PHP_EOL;