diff --git a/src/registrar/forms/domain.py b/src/registrar/forms/domain.py
index d14ed41ba..b93950df0 100644
--- a/src/registrar/forms/domain.py
+++ b/src/registrar/forms/domain.py
@@ -26,7 +26,14 @@ class DomainNameserverForm(forms.Form):
 
     server = forms.CharField(label="Name server", strip=True)
 
-    ip = forms.CharField(label="IP address", strip=True, required=False)
+    ip = forms.CharField(
+        label="IP address", 
+        strip=True, 
+        required=False,
+        validators=[
+            # TODO in progress
+        ],
+    )
 
 
 NameserverFormset = formset_factory(
diff --git a/src/registrar/models/domain.py b/src/registrar/models/domain.py
index 80bb1ab30..0b9139277 100644
--- a/src/registrar/models/domain.py
+++ b/src/registrar/models/domain.py
@@ -313,14 +313,14 @@ class Domain(TimeStampedModel, DomainHelper):
             NameserverError (if exception hit)
         Returns:
             None"""
-        if self.isSubdomain(nameserver) and (ip is None or ip == []):
+        if self.isSubdomain(nameserver) and (ip is None or ip == [] or ip != []):
             raise NameserverError(code=nsErrorCodes.MISSING_IP, nameserver=nameserver)
 
-        elif not self.isSubdomain(nameserver) and (ip is not None and ip != []):
+        elif not self.isSubdomain(nameserver) and (ip is not None and ip != [] and ip != ['']):
             raise NameserverError(
                 code=nsErrorCodes.GLUE_RECORD_NOT_ALLOWED, nameserver=nameserver, ip=ip
             )
-        elif ip is not None and ip != []:
+        elif ip is not None and ip != [] and ip != ['']:
             for addr in ip:
                 logger.info(f"ip address {addr}")
                 if not self._valid_ip_addr(addr):
diff --git a/src/registrar/templates/domain_nameservers.html b/src/registrar/templates/domain_nameservers.html
index 37fa1eb85..fffd4b8c0 100644
--- a/src/registrar/templates/domain_nameservers.html
+++ b/src/registrar/templates/domain_nameservers.html
@@ -16,7 +16,7 @@
 
   {% include "includes/required_fields.html" %}
 
-  <form class="usa-form usa-form--large" method="post" novalidate id="form-container">
+  <form class="usa-form usa-form--extra-large" method="post" novalidate id="form-container">
     {% csrf_token %}
     {{ formset.management_form }}
 
@@ -26,7 +26,7 @@
         <div class="tablet:grid-col-6">
           {% with sublabel_text="Example: ns"|concat:forloop.counter|concat:".example.com" %}
             {% if forloop.counter <= 2 %}
-              {% with attr_required=True %}
+              {% with attr_required=True add_group_class="usa-form-group--unstyled-error" %}
                 {% input_with_errors form.server %}
               {% endwith %}
             {% else %}
@@ -35,7 +35,7 @@
           {% endwith %}
         </div>
         <div class="tablet:grid-col-6">
-          {% with sublabel_text="Example: ns"|concat:forloop.counter|concat:".example.com" %}
+          {% with sublabel_text="Example: ns"|concat:forloop.counter|concat:".example.com" add_group_class="usa-form-group--unstyled-error" %}
             {% input_with_errors form.ip %}
           {% endwith %}
         </div>
diff --git a/src/registrar/views/domain.py b/src/registrar/views/domain.py
index dbf65fe6b..f8e144f7f 100644
--- a/src/registrar/views/domain.py
+++ b/src/registrar/views/domain.py
@@ -23,6 +23,7 @@ from registrar.models import (
     UserDomainRole,
 )
 from registrar.models.public_contact import PublicContact
+from registrar.utility.errors import NameserverError
 
 from ..forms import (
     ContactForm,
@@ -222,20 +223,44 @@ class DomainNameserversView(DomainPermissionView, FormMixin):
         nameservers = []
         for form in formset:
             try:
+                ip_string = form.cleaned_data["ip"]
+                # Split the string into a list using a comma as the delimiter
+                ip_list = ip_string.split(',')
+                # Remove any leading or trailing whitespace from each IP in the list
+                # this will return [''] if no ips have been entered, which is taken
+                # into account in the model in checkHostIPCombo
+                ip_list = [ip.strip() for ip in ip_list]
+                            
                 as_tuple = (
                     form.cleaned_data["server"],
-                    [form.cleaned_data["ip"]]
+                    ip_list,
                 )
                 nameservers.append(as_tuple)
             except KeyError:
                 # no server information in this field, skip it
                 pass
         domain = self.get_object()
-        domain.nameservers = nameservers
-
-        messages.success(
-            self.request, "The name servers for this domain have been updated."
-        )
+        
+        try:
+            domain.nameservers = nameservers
+        except NameserverError as Err:
+            # TODO: move into literal
+            messages.error(self.request, 'Whoops, Nameservers Error')
+            #  messages.error(self.request, GENERIC_ERROR)
+            logger.error(f"Nameservers error: {Err}")
+        # TODO: registry is not throwing an error when no connection
+        # TODO: merge 1103 and use literals
+        except RegistryError as Err:
+            if Err.is_connection_error():
+                messages.error(self.request, 'CANNOT_CONTACT_REGISTRY')
+                logger.error(f"Registry connection error: {Err}")
+            else:
+                messages.error(self.request, 'GENERIC_ERROR')
+                logger.error(f"Registry error: {Err}")
+        else:
+            messages.success(
+                self.request, "The name servers for this domain have been updated."
+            )
 
         # superclass has the redirect
         return super().form_valid(formset)