diff --git a/netbox/templates/virtualization/virtualmachine.html b/netbox/templates/virtualization/virtualmachine.html
index f14ba1c86..873f18158 100644
--- a/netbox/templates/virtualization/virtualmachine.html
+++ b/netbox/templates/virtualization/virtualmachine.html
@@ -145,12 +145,6 @@
                       <td>
                         {% if object.disk %}
                           {{ object.disk }} {% trans "GB" context "Abbreviation for gigabyte" %}
-                          <span class="text-warning">
-                            <i class="mdi mdi-alert" title="{% trans "This field has been deprecated and will be removed in a future release." %}"></i>
-                          </span>
-                        {% elif object.disk_size %}
-                          {{ object.disk_size }} {% trans "GB" context "Abbreviation for gigabyte" %}
-                          ({{ object.virtualdisks.count }} {% trans "disks" %})
                         {% else %}
                           {{ ''|placeholder }}
                         {% endif %}
diff --git a/netbox/virtualization/apps.py b/netbox/virtualization/apps.py
index 8db943ea1..f0af9a163 100644
--- a/netbox/virtualization/apps.py
+++ b/netbox/virtualization/apps.py
@@ -5,7 +5,7 @@ class VirtualizationConfig(AppConfig):
     name = 'virtualization'
 
     def ready(self):
-        from . import search
+        from . import search, signals
         from .models import VirtualMachine
         from utilities.counters import connect_counters
 
diff --git a/netbox/virtualization/forms/model_forms.py b/netbox/virtualization/forms/model_forms.py
index 6e108fedd..80794281b 100644
--- a/netbox/virtualization/forms/model_forms.py
+++ b/netbox/virtualization/forms/model_forms.py
@@ -240,6 +240,11 @@ class VirtualMachineForm(TenancyForm, NetBoxModelForm):
 
         if self.instance.pk:
 
+            # Disable the disk field if one or more VirtualDisks have been created
+            if self.instance.virtualdisks.exists():
+                self.fields['disk'].widget.attrs['disabled'] = True
+                self.fields['disk'].help_text = _("Disk size is managed via the attachment of virtual disks.")
+
             # Compile list of choices for primary IPv4 and IPv6 addresses
             for family in [4, 6]:
                 ip_choices = [(None, '---------')]
diff --git a/netbox/virtualization/models/virtualmachines.py b/netbox/virtualization/models/virtualmachines.py
index 970167bf3..634c59c9e 100644
--- a/netbox/virtualization/models/virtualmachines.py
+++ b/netbox/virtualization/models/virtualmachines.py
@@ -2,7 +2,7 @@ from django.contrib.contenttypes.fields import GenericRelation
 from django.core.exceptions import ValidationError
 from django.core.validators import MinValueValidator
 from django.db import models
-from django.db.models import Q
+from django.db.models import Q, Sum
 from django.db.models.functions import Lower
 from django.urls import reverse
 from django.utils.translation import gettext_lazy as _
@@ -120,12 +120,10 @@ class VirtualMachine(ContactsMixin, RenderConfigMixin, ConfigContextModel, Prima
         null=True,
         verbose_name=_('memory (MB)')
     )
-    # TODO: Remove in v4.0
     disk = models.PositiveIntegerField(
         blank=True,
         null=True,
-        verbose_name=_('disk (GB)'),
-        help_text=_('deprecated - use Virtual Disks')
+        verbose_name=_('disk (GB)')
     )
 
     # Counter fields
@@ -199,6 +197,17 @@ class VirtualMachine(ContactsMixin, RenderConfigMixin, ConfigContextModel, Prima
                 ).format(device=self.device, cluster=self.cluster)
             })
 
+        # Validate aggregate disk size
+        if self.pk:
+            total_disk = self.virtualdisks.aggregate(Sum('size', default=0))['size__sum']
+            if total_disk and self.disk != total_disk:
+                raise ValidationError({
+                    'disk': _(
+                        "The specified disk size ({size}) must match the aggregate size of assigned virtual disks "
+                        "({total_size})."
+                    ).format(size=self.disk, total_size=total_disk)
+                })
+
         # Validate primary IP addresses
         interfaces = self.interfaces.all() if self.pk else None
         for family in (4, 6):
diff --git a/netbox/virtualization/signals.py b/netbox/virtualization/signals.py
new file mode 100644
index 000000000..2ee015211
--- /dev/null
+++ b/netbox/virtualization/signals.py
@@ -0,0 +1,16 @@
+from django.db.models import Sum
+from django.db.models.signals import post_delete, post_save
+from django.dispatch import receiver
+
+from .models import VirtualDisk, VirtualMachine
+
+
+@receiver((post_delete, post_save), sender=VirtualDisk)
+def update_circuit(instance, **kwargs):
+    """
+    When a VirtualDisk has been modified, update the aggregate disk_size value of its VM.
+    """
+    vm = instance.virtual_machine
+    VirtualMachine.objects.filter(pk=vm.pk).update(
+        disk=vm.virtualdisks.aggregate(Sum('size'))['size__sum']
+    )
diff --git a/netbox/virtualization/tests/test_models.py b/netbox/virtualization/tests/test_models.py
index 782b9f07f..c94ff930e 100644
--- a/netbox/virtualization/tests/test_models.py
+++ b/netbox/virtualization/tests/test_models.py
@@ -90,3 +90,28 @@ class VirtualMachineTestCase(TestCase):
         # Uniqueness validation for name should ignore case
         with self.assertRaises(ValidationError):
             vm2.full_clean()
+
+    def test_disk_size(self):
+        vm = VirtualMachine(
+            cluster=Cluster.objects.first(),
+            name='Virtual Machine 1'
+        )
+        vm.save()
+        vm.refresh_from_db()
+        self.assertEqual(vm.disk, None)
+
+        # Create two VirtualDisks
+        VirtualDisk.objects.create(virtual_machine=vm, name='Virtual Disk 1', size=10)
+        VirtualDisk.objects.create(virtual_machine=vm, name='Virtual Disk 2', size=10)
+        vm.refresh_from_db()
+        self.assertEqual(vm.disk, 20)
+
+        # Delete one VirtualDisk
+        VirtualDisk.objects.first().delete()
+        vm.refresh_from_db()
+        self.assertEqual(vm.disk, 10)
+
+        # Attempt to manually overwrite the aggregate disk size
+        vm.disk = 30
+        with self.assertRaises(ValidationError):
+            vm.full_clean()