diff --git a/netbox/dcim/forms/model_forms.py b/netbox/dcim/forms/model_forms.py
index 92e0f30ae..76faa54ba 100644
--- a/netbox/dcim/forms/model_forms.py
+++ b/netbox/dcim/forms/model_forms.py
@@ -1705,6 +1705,22 @@ class VirtualDeviceContextForm(TenancyForm, NetBoxModelForm):
             'rack_id': '$rack',
         }
     )
+    primary_ip4 = DynamicModelChoiceField(
+        queryset=IPAddress.objects.all(),
+        required=False,
+        query_params={
+            'device_id': '$device',
+            'family': 4,
+        }
+    )
+    primary_ip6 = DynamicModelChoiceField(
+        queryset=IPAddress.objects.all(),
+        required=False,
+        query_params={
+            'device_id': '$device',
+            'family': 6,
+        }
+    )
 
     fieldsets = (
         ('Assigned Device', ('region', 'site_group', 'site', 'location', 'rack', 'device')),
@@ -1720,6 +1736,4 @@ class VirtualDeviceContextForm(TenancyForm, NetBoxModelForm):
         ]
         widgets = {
             'status': StaticSelect(),
-            'primary_ip4': StaticSelect(),
-            'primary_ip6': StaticSelect(),
         }
diff --git a/netbox/dcim/models/devices.py b/netbox/dcim/models/devices.py
index 8b03015be..1e6581f8d 100644
--- a/netbox/dcim/models/devices.py
+++ b/netbox/dcim/models/devices.py
@@ -1175,3 +1175,25 @@ class VirtualDeviceContext(PrimaryModel):
             return self.primary_ip4
         else:
             return None
+
+    def clean(self):
+        super().clean()
+        vc_interfaces = self.device.vc_interfaces(if_master=False)
+        if self.primary_ip4:
+            if self.primary_ip4.family != 4:
+                raise ValidationError({
+                    'primary_ip4': f"{self.primary_ip4} is not an IPv4 address."
+                })
+            if self.primary_ip4.assigned_object not in vc_interfaces:
+                raise ValidationError({
+                    'primary_ip4': f"The specified IP address ({self.primary_ip4}) is not assigned to this device."
+                })
+        if self.primary_ip6:
+            if self.primary_ip6.family != 6:
+                raise ValidationError({
+                    'primary_ip6': f"{self.primary_ip6} is not an IPv6 address."
+                })
+            if self.primary_ip6.assigned_object not in vc_interfaces:
+                raise ValidationError({
+                    'primary_ip6': f"The specified IP address ({self.primary_ip6}) is not assigned to this device."
+                })
diff --git a/netbox/ipam/models/ip.py b/netbox/ipam/models/ip.py
index 20530d66c..d5efcdc7f 100644
--- a/netbox/ipam/models/ip.py
+++ b/netbox/ipam/models/ip.py
@@ -9,7 +9,7 @@ from django.utils.functional import cached_property
 from django.utils.translation import gettext as _
 
 from dcim.fields import ASNField
-from dcim.models import Device
+from dcim.models import Device, VirtualDeviceContext
 from ipam.choices import *
 from ipam.constants import *
 from ipam.fields import IPNetworkField, IPAddressField
@@ -866,7 +866,7 @@ class IPAddress(PrimaryModel):
 
         # Check for primary IP assignment that doesn't match the assigned device/VM
         if self.pk:
-            for cls, attr in ((Device, 'device'), (VirtualMachine, 'virtual_machine')):
+            for cls, attr in ((Device, 'device'), (VirtualMachine, 'virtual_machine'), (VirtualDeviceContext, 'device')):
                 parent = cls.objects.filter(Q(primary_ip4=self) | Q(primary_ip6=self)).first()
                 if parent and getattr(self.assigned_object, attr, None) != parent:
                     # Check for a NAT relationship