diff --git a/internal/core/vagrantfile.go b/internal/core/vagrantfile.go
index c2c9251e8..9fc8eb935 100644
--- a/internal/core/vagrantfile.go
+++ b/internal/core/vagrantfile.go
@@ -7,6 +7,7 @@ import (
 
 	"github.com/hashicorp/go-argmapper"
 	"github.com/hashicorp/go-hclog"
+	"github.com/pkg/errors"
 	"google.golang.org/grpc/codes"
 	"google.golang.org/grpc/status"
 	"google.golang.org/protobuf/proto"
@@ -18,6 +19,7 @@ import (
 	"github.com/hashicorp/vagrant-plugin-sdk/internal-shared/cleanup"
 	"github.com/hashicorp/vagrant-plugin-sdk/internal-shared/dynamic"
 	"github.com/hashicorp/vagrant-plugin-sdk/internal-shared/protomappers"
+	"github.com/hashicorp/vagrant-plugin-sdk/localizer"
 	"github.com/hashicorp/vagrant-plugin-sdk/proto/vagrant_plugin_sdk"
 	"github.com/hashicorp/vagrant/internal/plugin"
 	"github.com/hashicorp/vagrant/internal/server/proto/vagrant_server"
@@ -444,7 +446,7 @@ func (v *Vagrantfile) Target(
 		return nil, err
 	}
 
-	conf, err := v.TargetConfig(name, provider, false)
+	conf, err := v.TargetConfig(name, provider, true)
 	if err != nil {
 		return
 	}
@@ -496,7 +498,6 @@ func (v *Vagrantfile) Target(
 
 // Generate a new Vagrantfile for the given target
 // NOTE: This function may return a nil result without an error
-// TODO(spox): Provider validation is not currently implemented
 // TODO(spox): Needs box configuration applied
 func (v *Vagrantfile) TargetConfig(
 	name, // name of the target
@@ -511,6 +512,29 @@ func (v *Vagrantfile) TargetConfig(
 		return nil, err
 	}
 
+	if provider != "" {
+		pp, err := v.factory.plugins.Find(provider, component.ProviderType)
+		if err != nil {
+			return nil, err
+		}
+		if validateProvider {
+			usable, err := pp.Component.(core.Provider).Usable()
+			if err != nil {
+				return nil, err
+			}
+			if !usable {
+				// TODO: include message provided in the error
+				return nil, errors.New(
+					localizer.LocalizeMsg(
+						"provider_not_usable",
+						map[string]string{"Provider": provider, "Machine": name},
+					),
+				)
+
+			}
+		}
+	}
+
 	cid := name + "+" + provider
 	if cv := v.cache.Get(cid); cv != nil {
 		return cv.(core.Vagrantfile), nil
diff --git a/plugins/commands/serve/service/provider_service.rb b/plugins/commands/serve/service/provider_service.rb
index e978645ca..cf66efe38 100644
--- a/plugins/commands/serve/service/provider_service.rb
+++ b/plugins/commands/serve/service/provider_service.rb
@@ -20,7 +20,7 @@ module VagrantPlugins
 
         def usable(req, ctx)
           with_plugin(ctx, :providers, broker: broker) do |plugin|
-            is_usable = plugin.usable?
+            is_usable = plugin.usable?(true)
             SDK::Provider::UsableResp.new(
               is_usable: is_usable,
             )