diff --git a/nixos/maintainers/scripts/ec2/amazon-image.nix b/nixos/maintainers/scripts/ec2/amazon-image.nix
index 9d0e7f5883e0..e08cf572f7f9 100644
--- a/nixos/maintainers/scripts/ec2/amazon-image.nix
+++ b/nixos/maintainers/scripts/ec2/amazon-image.nix
@@ -15,11 +15,23 @@ let
   inherit (lib.options) literalExpression;
   cfg = config.amazonImage;
   amiBootMode = if config.ec2.efi then "uefi" else "legacy-bios";
-
 in
 {
-
-  imports = [ ../../../modules/virtualisation/amazon-image.nix ];
+  imports = [
+    ../../../modules/virtualisation/amazon-image.nix
+    ../../../modules/virtualisation/disk-size-option.nix
+    (lib.mkRenamedOptionModuleWith {
+      sinceRelease = 2411;
+      from = [
+        "amazonImage"
+        "sizeMB"
+      ];
+      to = [
+        "virtualisation"
+        "diskSize"
+      ];
+    })
+  ];
 
   # Amazon recommends setting this to the highest possible value for a good EBS
   # experience, which prior to 4.15 was 255.
@@ -52,13 +64,6 @@ in
       '';
     };
 
-    sizeMB = mkOption {
-      type = with types; either (enum [ "auto" ]) int;
-      default = 3072;
-      example = 8192;
-      description = "The size in MB of the image";
-    };
-
     format = mkOption {
       type = types.enum [
         "raw"
@@ -70,6 +75,11 @@ in
     };
   };
 
+  # Use a priority just below mkOptionDefault (1500) instead of lib.mkDefault
+  # to avoid breaking existing configs using that.
+  config.virtualisation.diskSize = lib.mkOverride 1490 (3 * 1024);
+  config.virtualisation.diskSizeAutoSupported = !config.ec2.zfs.enable;
+
   config.system.build.amazonImage =
     let
       configFile = pkgs.writeText "configuration.nix" ''
@@ -98,7 +108,7 @@ in
 
         bootSize = 1000; # 1G is the minimum EBS volume
 
-        rootSize = cfg.sizeMB;
+        rootSize = config.virtualisation.diskSize;
         rootPoolProperties = {
           ashift = 12;
           autoexpand = "on";
@@ -151,7 +161,7 @@ in
         fsType = "ext4";
         partitionTableType = if config.ec2.efi then "efi" else "legacy+gpt";
 
-        diskSize = cfg.sizeMB;
+        inherit (config.virtualisation) diskSize;
 
         postVM = ''
            extension=''${diskImage##*.}
diff --git a/nixos/maintainers/scripts/openstack/openstack-image-zfs.nix b/nixos/maintainers/scripts/openstack/openstack-image-zfs.nix
index 72f123b16229..57022bd2f784 100644
--- a/nixos/maintainers/scripts/openstack/openstack-image-zfs.nix
+++ b/nixos/maintainers/scripts/openstack/openstack-image-zfs.nix
@@ -15,6 +15,18 @@ in
 {
   imports = [
     ../../../modules/virtualisation/openstack-config.nix
+    ../../../modules/virtualisation/disk-size-option.nix
+    (lib.mkRenamedOptionModuleWith {
+      sinceRelease = 2411;
+      from = [
+        "openstackImage"
+        "sizeMB"
+      ];
+      to = [
+        "virtualisation"
+        "diskSize"
+      ];
+    })
   ] ++ (lib.optional copyChannel ../../../modules/installer/cd-dvd/channel.nix);
 
   options.openstackImage = {
@@ -26,16 +38,10 @@ in
 
     ramMB = mkOption {
       type = types.int;
-      default = 1024;
+      default = (3 * 1024);
       description = "RAM allocation for build VM";
     };
 
-    sizeMB = mkOption {
-      type = types.int;
-      default = 8192;
-      description = "The size in MB of the image";
-    };
-
     format = mkOption {
       type = types.enum [
         "raw"
@@ -61,6 +67,11 @@ in
       };
     };
 
+    # Use a priority just below mkOptionDefault (1500) instead of lib.mkDefault
+    # to avoid breaking existing configs using that.
+    virtualisation.diskSize = lib.mkOverride 1490 (8 * 1024);
+    virtualisation.diskSizeAutoSupported = false;
+
     system.build.openstackImage = import ../../../lib/make-single-disk-zfs-image.nix {
       inherit lib config;
       inherit (cfg) contents format name;
@@ -77,7 +88,7 @@ in
 
       bootSize = 1000;
       memSize = cfg.ramMB;
-      rootSize = cfg.sizeMB;
+      rootSize = config.virtualisation.diskSize;
       rootPoolProperties = {
         ashift = 12;
         autoexpand = "on";
diff --git a/nixos/modules/virtualisation/azure-image.nix b/nixos/modules/virtualisation/azure-image.nix
index 1f6b2bd52c04..76d8a3bb365b 100644
--- a/nixos/modules/virtualisation/azure-image.nix
+++ b/nixos/modules/virtualisation/azure-image.nix
@@ -10,18 +10,24 @@ let
   cfg = config.virtualisation.azureImage;
 in
 {
-  imports = [ ./azure-common.nix ];
+  imports = [
+    ./azure-common.nix
+    ./disk-size-option.nix
+    (lib.mkRenamedOptionModuleWith {
+      sinceRelease = 2411;
+      from = [
+        "virtualisation"
+        "azureImage"
+        "diskSize"
+      ];
+      to = [
+        "virtualisation"
+        "diskSize"
+      ];
+    })
+  ];
 
   options.virtualisation.azureImage = {
-    diskSize = mkOption {
-      type = with types; either (enum [ "auto" ]) int;
-      default = "auto";
-      example = 2048;
-      description = ''
-        Size of disk image. Unit is MB.
-      '';
-    };
-
     bootSize = mkOption {
       type = types.int;
       default = 256;
@@ -67,7 +73,8 @@ in
       bootSize = "${toString cfg.bootSize}M";
       partitionTableType = if cfg.vmGeneration == "v2" then "efi" else "legacy";
 
-      inherit (cfg) diskSize contents;
+      inherit (cfg) contents;
+      inherit (config.virtualisation) diskSize;
       inherit config lib pkgs;
     };
   };
diff --git a/nixos/modules/virtualisation/digital-ocean-image.nix b/nixos/modules/virtualisation/digital-ocean-image.nix
index 2d06c4c38fa1..b6ef01516e34 100644
--- a/nixos/modules/virtualisation/digital-ocean-image.nix
+++ b/nixos/modules/virtualisation/digital-ocean-image.nix
@@ -11,18 +11,24 @@ let
 in
 {
 
-  imports = [ ./digital-ocean-config.nix ];
+  imports = [
+    ./digital-ocean-config.nix
+    ./disk-size-option.nix
+    (lib.mkRenamedOptionModuleWith {
+      sinceRelease = 2411;
+      from = [
+        "virtualisation"
+        "digitalOceanImage"
+        "diskSize"
+      ];
+      to = [
+        "virtualisation"
+        "diskSize"
+      ];
+    })
+  ];
 
   options = {
-    virtualisation.digitalOceanImage.diskSize = mkOption {
-      type = with types; either (enum [ "auto" ]) int;
-      default = "auto";
-      example = 4096;
-      description = ''
-        Size of disk image. Unit is MB.
-      '';
-    };
-
     virtualisation.digitalOceanImage.configFile = mkOption {
       type = with types; nullOr path;
       default = null;
@@ -52,7 +58,6 @@ in
 
   #### implementation
   config = {
-
     system.build.digitalOceanImage = import ../../lib/make-disk-image.nix {
       name = "digital-ocean-image";
       format = "qcow2";
@@ -73,7 +78,7 @@ in
           config.virtualisation.digitalOcean.defaultConfigFile
         else
           cfg.configFile;
-      inherit (cfg) diskSize;
+      inherit (config.virtualisation) diskSize;
       inherit config lib pkgs;
     };
 
diff --git a/nixos/modules/virtualisation/disk-size-option.nix b/nixos/modules/virtualisation/disk-size-option.nix
new file mode 100644
index 000000000000..487c3adfe2b7
--- /dev/null
+++ b/nixos/modules/virtualisation/disk-size-option.nix
@@ -0,0 +1,38 @@
+{ lib, config, ... }:
+let
+  t = lib.types;
+in
+{
+  options = {
+    virtualisation.diskSizeAutoSupported = lib.mkOption {
+      type = t.bool;
+      default = true;
+      description = ''
+        Whether the current image builder or vm runner supports `virtualisation.diskSize = "auto".`
+      '';
+      internal = true;
+    };
+
+    virtualisation.diskSize = lib.mkOption {
+      type = t.either (t.enum [ "auto" ]) t.ints.positive;
+      default = if config.virtualisation.diskSizeAutoSupported then "auto" else 1024;
+      defaultText = "\"auto\" if diskSizeAutoSupported, else 1024";
+      description = ''
+        The disk size in megabytes of the virtual machine.
+      '';
+    };
+  };
+
+  config =
+    let
+      inherit (config.virtualisation) diskSize diskSizeAutoSupported;
+    in
+    {
+      assertions = [
+        {
+          assertion = diskSize != "auto" || diskSizeAutoSupported;
+          message = "Setting virtualisation.diskSize to `auto` is not supported by the current image build or vm runner; use an explicit size.";
+        }
+      ];
+    };
+}
diff --git a/nixos/modules/virtualisation/google-compute-image.nix b/nixos/modules/virtualisation/google-compute-image.nix
index 416b47b768d9..c2529bb3db3f 100644
--- a/nixos/modules/virtualisation/google-compute-image.nix
+++ b/nixos/modules/virtualisation/google-compute-image.nix
@@ -19,18 +19,24 @@ let
 in
 {
 
-  imports = [ ./google-compute-config.nix ];
+  imports = [
+    ./google-compute-config.nix
+    ./disk-size-option.nix
+    (lib.mkRenamedOptionModuleWith {
+      sinceRelease = 2411;
+      from = [
+        "virtualisation"
+        "googleComputeImage"
+        "diskSize"
+      ];
+      to = [
+        "virtualisation"
+        "diskSize"
+      ];
+    })
+  ];
 
   options = {
-    virtualisation.googleComputeImage.diskSize = mkOption {
-      type = with types; either (enum [ "auto" ]) int;
-      default = "auto";
-      example = 1536;
-      description = ''
-        Size of disk image. Unit is MB.
-      '';
-    };
-
     virtualisation.googleComputeImage.configFile = mkOption {
       type = with types; nullOr str;
       default = null;
@@ -86,7 +92,7 @@ in
       format = "raw";
       configFile = if cfg.configFile == null then defaultConfigFile else cfg.configFile;
       partitionTableType = if cfg.efi then "efi" else "legacy";
-      inherit (cfg) diskSize;
+      inherit (config.virtualisation) diskSize;
       inherit config lib pkgs;
     };
 
diff --git a/nixos/modules/virtualisation/hyperv-image.nix b/nixos/modules/virtualisation/hyperv-image.nix
index d4ed256d0d91..ea0603fa6ae5 100644
--- a/nixos/modules/virtualisation/hyperv-image.nix
+++ b/nixos/modules/virtualisation/hyperv-image.nix
@@ -9,19 +9,26 @@ with lib;
 
 let
   cfg = config.hyperv;
-
 in
 {
+
+  imports = [
+    ./disk-size-option.nix
+    (lib.mkRenamedOptionModuleWith {
+      sinceRelease = 2411;
+      from = [
+        "hyperv"
+        "baseImageSize"
+      ];
+      to = [
+        "virtualisation"
+        "diskSize"
+      ];
+    })
+  ];
+
   options = {
     hyperv = {
-      baseImageSize = mkOption {
-        type = with types; either (enum [ "auto" ]) int;
-        default = "auto";
-        example = 2048;
-        description = ''
-          The size of the hyper-v base image in MiB.
-        '';
-      };
       vmDerivationName = mkOption {
         type = types.str;
         default = "nixos-hyperv-${config.system.nixos.label}-${pkgs.stdenv.hostPlatform.system}";
@@ -40,6 +47,10 @@ in
   };
 
   config = {
+    # Use a priority just below mkOptionDefault (1500) instead of lib.mkDefault
+    # to avoid breaking existing configs using that.
+    virtualisation.diskSize = lib.mkOverride 1490 (4 * 1024);
+
     system.build.hypervImage = import ../../lib/make-disk-image.nix {
       name = cfg.vmDerivationName;
       postVM = ''
@@ -47,7 +58,7 @@ in
         rm $diskImage
       '';
       format = "raw";
-      diskSize = cfg.baseImageSize;
+      inherit (config.virtualisation) diskSize;
       partitionTableType = "efi";
       inherit config lib pkgs;
     };
diff --git a/nixos/modules/virtualisation/linode-image.nix b/nixos/modules/virtualisation/linode-image.nix
index 48d7f98e6abe..ff61c5f5d1db 100644
--- a/nixos/modules/virtualisation/linode-image.nix
+++ b/nixos/modules/virtualisation/linode-image.nix
@@ -17,17 +17,24 @@ let
   '';
 in
 {
-  imports = [ ./linode-config.nix ];
+  imports = [
+    ./linode-config.nix
+    ./disk-size-option.nix
+    (lib.mkRenamedOptionModuleWith {
+      sinceRelease = 2411;
+      from = [
+        "virtualisation"
+        "linodeImage"
+        "diskSize"
+      ];
+      to = [
+        "virtualisation"
+        "diskSize"
+      ];
+    })
+  ];
 
   options = {
-    virtualisation.linodeImage.diskSize = mkOption {
-      type = with types; either (enum (singleton "auto")) ints.positive;
-      default = "auto";
-      example = 1536;
-      description = ''
-        Size of disk image in MB.
-      '';
-    };
 
     virtualisation.linodeImage.configFile = mkOption {
       type = with types; nullOr str;
@@ -62,7 +69,7 @@ in
       format = "raw";
       partitionTableType = "none";
       configFile = if cfg.configFile == null then defaultConfigFile else cfg.configFile;
-      inherit (cfg) diskSize;
+      inherit (config.virtualisation) diskSize;
       inherit config lib pkgs;
     };
   };
diff --git a/nixos/modules/virtualisation/oci-image.nix b/nixos/modules/virtualisation/oci-image.nix
index b867e7ae30e7..fe286853de81 100644
--- a/nixos/modules/virtualisation/oci-image.nix
+++ b/nixos/modules/virtualisation/oci-image.nix
@@ -12,9 +12,14 @@ in
   imports = [ ./oci-common.nix ];
 
   config = {
+    # Use a priority just below mkOptionDefault (1500) instead of lib.mkDefault
+    # to avoid breaking existing configs using that.
+    virtualisation.diskSize = lib.mkOverride 1490 (8 * 1024);
+    virtualisation.diskSizeAutoSupported = false;
+
     system.build.OCIImage = import ../../lib/make-disk-image.nix {
       inherit config lib pkgs;
-      inherit (cfg) diskSize;
+      inherit (config.virtualisation) diskSize;
       name = "oci-image";
       configFile = ./oci-config-user.nix;
       format = "qcow2";
diff --git a/nixos/modules/virtualisation/oci-options.nix b/nixos/modules/virtualisation/oci-options.nix
index 629b651ca5ac..b8d66c0290b3 100644
--- a/nixos/modules/virtualisation/oci-options.nix
+++ b/nixos/modules/virtualisation/oci-options.nix
@@ -1,10 +1,23 @@
 {
-  config,
   lib,
-  pkgs,
   ...
 }:
 {
+  imports = [
+    ./disk-size-option.nix
+    (lib.mkRenamedOptionModuleWith {
+      sinceRelease = 2411;
+      from = [
+        "oci"
+        "diskSize"
+      ];
+      to = [
+        "virtualisation"
+        "diskSize"
+      ];
+    })
+  ];
+
   options = {
     oci = {
       efi = lib.mkOption {
@@ -14,12 +27,6 @@
           Whether the OCI instance is using EFI.
         '';
       };
-      diskSize = lib.mkOption {
-        type = lib.types.int;
-        default = 8192;
-        description = "Size of the disk image created in MB.";
-        example = "diskSize = 12 * 1024; # 12GiB";
-      };
     };
   };
 }
diff --git a/nixos/modules/virtualisation/proxmox-image.nix b/nixos/modules/virtualisation/proxmox-image.nix
index 4364fbff2a83..9bbe7a596f07 100644
--- a/nixos/modules/virtualisation/proxmox-image.nix
+++ b/nixos/modules/virtualisation/proxmox-image.nix
@@ -6,8 +6,23 @@
 }:
 
 with lib;
-
 {
+  imports = [
+    ./disk-size-option.nix
+    (lib.mkRenamedOptionModuleWith {
+      sinceRelease = 2411;
+      from = [
+        "proxmox"
+        "qemuConf"
+        "diskSize"
+      ];
+      to = [
+        "virtualisation"
+        "diskSize"
+      ];
+    })
+  ];
+
   options.proxmox = {
     qemuConf = {
       # essential configs
@@ -95,16 +110,6 @@ with lib;
           either "efi" or "hybrid".
         '';
       };
-      diskSize = mkOption {
-        type = types.str;
-        default = "auto";
-        example = "20480";
-        description = ''
-          The size of the disk, in megabytes.
-          if "auto" size is calculated based on the contents copied to it and
-          additionalSpace is taken into account.
-        '';
-      };
       net0 = mkOption {
         type = types.commas;
         default = "virtio=00:00:00:00:00:00,bridge=vmbr0,firewall=1";
@@ -305,7 +310,8 @@ with lib;
             mkdir -p $out/nix-support
             echo "file vma $out/vzdump-qemu-${cfg.filenameSuffix}.vma.zst" > $out/nix-support/hydra-build-products
           '';
-        inherit (cfg.qemuConf) additionalSpace diskSize bootSize;
+        inherit (cfg.qemuConf) additionalSpace bootSize;
+        inherit (config.virtualisation) diskSize;
         format = "raw";
         inherit config lib pkgs;
       };
diff --git a/nixos/modules/virtualisation/qemu-vm.nix b/nixos/modules/virtualisation/qemu-vm.nix
index fe803c1971ca..af2f13b003a4 100644
--- a/nixos/modules/virtualisation/qemu-vm.nix
+++ b/nixos/modules/virtualisation/qemu-vm.nix
@@ -317,12 +317,11 @@ let
     copyChannel = false;
     OVMF = cfg.efi.OVMF;
   };
-
 in
-
 {
   imports = [
     ../profiles/qemu-guest.nix
+    ./disk-size-option.nix
     (mkRenamedOptionModule
       [
         "virtualisation"
@@ -378,14 +377,6 @@ in
       '';
     };
 
-    virtualisation.diskSize = mkOption {
-      type = types.ints.positive;
-      default = 1024;
-      description = ''
-        The disk size in megabytes of the virtual machine.
-      '';
-    };
-
     virtualisation.diskImage = mkOption {
       type = types.nullOr types.str;
       default = "./${config.system.name}.qcow2";
@@ -1250,6 +1241,8 @@ in
     # override by setting `virtualisation.fileSystems = lib.mkForce { };`.
     fileSystems = lib.mkIf (cfg.fileSystems != { }) (mkVMOverride cfg.fileSystems);
 
+    virtualisation.diskSizeAutoSupported = false;
+
     virtualisation.fileSystems =
       let
         mkSharedDir = tag: share: {
diff --git a/nixos/modules/virtualisation/virtualbox-image.nix b/nixos/modules/virtualisation/virtualbox-image.nix
index 968f5b766e87..22646011d33d 100644
--- a/nixos/modules/virtualisation/virtualbox-image.nix
+++ b/nixos/modules/virtualisation/virtualbox-image.nix
@@ -7,22 +7,27 @@
 let
 
   cfg = config.virtualbox;
-
 in
 {
+  imports = [
+    ./disk-size-option.nix
+    (lib.mkRenamedOptionModuleWith {
+      sinceRelease = 2411;
+      from = [
+        "virtualbox"
+        "baseImageSize"
+      ];
+      to = [
+        "virtualisation"
+        "diskSize"
+      ];
+    })
+  ];
 
   options = {
     virtualbox = {
-      baseImageSize = lib.mkOption {
-        type = with lib.types; either (enum [ "auto" ]) int;
-        default = "auto";
-        example = 50 * 1024;
-        description = ''
-          The size of the VirtualBox base image in MiB.
-        '';
-      };
       baseImageFreeSpace = lib.mkOption {
-        type = with lib.types; int;
+        type = lib.types.int;
         default = 30 * 1024;
         description = ''
           Free space in the VirtualBox base image in MiB.
@@ -180,6 +185,9 @@ in
   };
 
   config = {
+    # Use a priority just below mkOptionDefault (1500) instead of lib.mkDefault
+    # to avoid breaking existing configs using that.
+    virtualisation.diskSize = lib.mkOverride 1490 (50 * 1024);
 
     virtualbox.params = lib.mkMerge [
       (lib.mapAttrs (name: lib.mkDefault) {
@@ -204,7 +212,7 @@ in
 
       inherit pkgs lib config;
       partitionTableType = "legacy";
-      diskSize = cfg.baseImageSize;
+      inherit (config.virtualisation) diskSize;
       additionalSpace = "${toString cfg.baseImageFreeSpace}M";
 
       postVM = ''
diff --git a/nixos/release.nix b/nixos/release.nix
index 8a8c45f8f842..f77b9983e496 100644
--- a/nixos/release.nix
+++ b/nixos/release.nix
@@ -312,7 +312,7 @@ in rec {
         [ configuration
           versionModule
           ./maintainers/scripts/ec2/amazon-image.nix
-          ({ ... }: { amazonImage.sizeMB = "auto"; })
+          ({ ... }: { amazonImage.virtualisation.diskSize = "auto"; })
         ];
     }).config.system.build.amazonImage)