diff --git a/api/error.gen.go b/api/error.gen.go
index 9af1599bea..094dd067f0 100644
--- a/api/error.gen.go
+++ b/api/error.gen.go
@@ -13,7 +13,7 @@ type Error struct {
 	defaultFields []string
 
 	// The HTTP Status code applicable to this error
-	Status *int64 `json:"status,omitempty"`
+	Status *int32 `json:"status,omitempty"`
 	// An application-specific error string
 	Code *string `json:"code,omitempty"`
 	// A human readable explanation specific to this occurrence of the error
diff --git a/api/internal/genapi/parse.go b/api/internal/genapi/parse.go
index 6c901bf69b..2db7fc5a31 100644
--- a/api/internal/genapi/parse.go
+++ b/api/internal/genapi/parse.go
@@ -222,9 +222,7 @@ func parsePBs() {
 				}
 
 			TAGMODIFY:
-				// TraceId needs to be handled differently because it's a
-				// specific value used by OpenTelemetry
-				st.Fields.List[i].Tag.Value = "`" + strings.Replace(regex.FindString(st.Fields.List[i].Tag.Value), "trace_id", "TraceId", 1) + "`"
+				st.Fields.List[i].Tag.Value = "`" + regex.FindString(st.Fields.List[i].Tag.Value) + "`"
 			}
 		}), inAst)
 
diff --git a/api/scopes/project_test.go b/api/scopes/project_test.go
index 63f1694228..93fa256422 100644
--- a/api/scopes/project_test.go
+++ b/api/scopes/project_test.go
@@ -1,6 +1,7 @@
 package scopes
 
 import (
+	"net/http"
 	"testing"
 
 	"github.com/hashicorp/watchtower/api"
@@ -43,7 +44,32 @@ func TestProjects_Crud(t *testing.T) {
 	existed, apiErr, err = org.DeleteProject(tc.Context(), p)
 	assert.NoError(t, err)
 	assert.False(t, existed, "Expected project to not exist when deleted, but it did.")
+}
+
+// TODO: Get better coverage for expected errors and error formats.
+func TestProject_Errors(t *testing.T) {
+	assert := assert.New(t)
+	tc := controller.NewTestController(t, nil)
+	defer tc.Shutdown()
+	ctx := tc.Context()
+
+	client := tc.Client()
+	org := &Organization{
+		Client: client,
+	}
+	createdProj, apiErr, err := org.CreateProject(ctx, &Project{})
+	assert.NoError(err)
+	assert.NotNil(createdProj)
+	assert.Nil(apiErr)
+
+	_, apiErr, err = org.ReadProject(ctx, &Project{Id: "p_doesntexis"})
+	assert.NoError(err)
+	// TODO: Should this be nil instead of just a Project that has no values set
+	assert.NotNil(apiErr)
+	assert.EqualValues(*apiErr.Status, http.StatusNotFound)
 
-	// TODO: Error conditions once the proper errors are being returned.
-	// Probably as parallel subtests against the same DB.
+	_, apiErr, err = org.ReadProject(ctx, &Project{Id: "invalid id"})
+	assert.NoError(err)
+	assert.NotNil(apiErr)
+	assert.EqualValues(*apiErr.Status, http.StatusBadRequest)
 }
diff --git a/api/util.go b/api/util.go
index d9deb10228..1aa359fe21 100644
--- a/api/util.go
+++ b/api/util.go
@@ -30,15 +30,15 @@ func StringOrNil(in string) *string {
 }
 
 // Int returns the given int64 as an int64 pointer
-func Int(in int64) *int64 {
-	ret := new(int64)
+func Int(in int32) *int32 {
+	ret := new(int32)
 	*ret = in
 	return ret
 }
 
 // IntOrNil is like Int, but the returned pointer will be nil if the integer is
 // 0
-func IntOrNil(in int64) *int64 {
+func IntOrNil(in int32) *int32 {
 	if in == 0 {
 		return nil
 	}
diff --git a/buf.yaml b/buf.yaml
index 378ba99181..c8b4da311d 100644
--- a/buf.yaml
+++ b/buf.yaml
@@ -14,4 +14,6 @@ lint:
     ENUM_VALUE_PREFIX:
       - controller/api/view/v1/view.proto
     ENUM_ZERO_VALUE_SUFFIX:
-      - controller/api/view/v1/view.proto
\ No newline at end of file
+      - controller/api/view/v1/view.proto
+    FIELD_LOWER_SNAKE_CASE:
+      - controller/api/v1/error.proto
diff --git a/internal/gen/controller/api/error.pb.go b/internal/gen/controller/api/error.pb.go
index e14f98fe37..bc7479e4c0 100644
--- a/internal/gen/controller/api/error.pb.go
+++ b/internal/gen/controller/api/error.pb.go
@@ -8,7 +8,6 @@ package api
 
 import (
 	proto "github.com/golang/protobuf/proto"
-	wrappers "github.com/golang/protobuf/ptypes/wrappers"
 	protoreflect "google.golang.org/protobuf/reflect/protoreflect"
 	protoimpl "google.golang.org/protobuf/runtime/protoimpl"
 	reflect "reflect"
@@ -31,9 +30,9 @@ type ErrorDetails struct {
 	sizeCache     protoimpl.SizeCache
 	unknownFields protoimpl.UnknownFields
 
-	TraceId       *wrappers.StringValue `protobuf:"bytes,1,opt,name=trace_id,json=TraceId,proto3" json:"trace_id,omitempty"`
-	RequestId     *wrappers.StringValue `protobuf:"bytes,2,opt,name=request_id,proto3" json:"request_id,omitempty"`
-	RequestFields []string              `protobuf:"bytes,3,rep,name=request_fields,proto3" json:"request_fields,omitempty"`
+	TraceId       string   `protobuf:"bytes,1,opt,name=TraceId,proto3" json:"TraceId,omitempty"`
+	RequestId     string   `protobuf:"bytes,2,opt,name=request_id,proto3" json:"request_id,omitempty"`
+	RequestFields []string `protobuf:"bytes,3,rep,name=request_fields,proto3" json:"request_fields,omitempty"`
 }
 
 func (x *ErrorDetails) Reset() {
@@ -68,18 +67,18 @@ func (*ErrorDetails) Descriptor() ([]byte, []int) {
 	return file_controller_api_v1_error_proto_rawDescGZIP(), []int{0}
 }
 
-func (x *ErrorDetails) GetTraceId() *wrappers.StringValue {
+func (x *ErrorDetails) GetTraceId() string {
 	if x != nil {
 		return x.TraceId
 	}
-	return nil
+	return ""
 }
 
-func (x *ErrorDetails) GetRequestId() *wrappers.StringValue {
+func (x *ErrorDetails) GetRequestId() string {
 	if x != nil {
 		return x.RequestId
 	}
-	return nil
+	return ""
 }
 
 func (x *ErrorDetails) GetRequestFields() []string {
@@ -96,11 +95,11 @@ type Error struct {
 	unknownFields protoimpl.UnknownFields
 
 	// The HTTP Status code applicable to this error
-	Status *wrappers.Int64Value `protobuf:"bytes,1,opt,name=status,proto3" json:"status,omitempty"`
+	Status int32 `protobuf:"varint,1,opt,name=status,proto3" json:"status,omitempty"`
 	// An application-specific error string
-	Code *wrappers.StringValue `protobuf:"bytes,2,opt,name=code,proto3" json:"code,omitempty"`
+	Code string `protobuf:"bytes,2,opt,name=code,proto3" json:"code,omitempty"`
 	// A human readable explanation specific to this occurrence of the error
-	Message *wrappers.StringValue `protobuf:"bytes,3,opt,name=message,proto3" json:"message,omitempty"`
+	Message string `protobuf:"bytes,3,opt,name=message,proto3" json:"message,omitempty"`
 	// Additional metadata regarding the error. Depending on the error
 	// different fields will be populated.
 	Details *ErrorDetails `protobuf:"bytes,4,opt,name=details,proto3" json:"details,omitempty"`
@@ -138,25 +137,25 @@ func (*Error) Descriptor() ([]byte, []int) {
 	return file_controller_api_v1_error_proto_rawDescGZIP(), []int{1}
 }
 
-func (x *Error) GetStatus() *wrappers.Int64Value {
+func (x *Error) GetStatus() int32 {
 	if x != nil {
 		return x.Status
 	}
-	return nil
+	return 0
 }
 
-func (x *Error) GetCode() *wrappers.StringValue {
+func (x *Error) GetCode() string {
 	if x != nil {
 		return x.Code
 	}
-	return nil
+	return ""
 }
 
-func (x *Error) GetMessage() *wrappers.StringValue {
+func (x *Error) GetMessage() string {
 	if x != nil {
 		return x.Message
 	}
-	return nil
+	return ""
 }
 
 func (x *Error) GetDetails() *ErrorDetails {
@@ -172,39 +171,27 @@ var file_controller_api_v1_error_proto_rawDesc = []byte{
 	0x0a, 0x1d, 0x63, 0x6f, 0x6e, 0x74, 0x72, 0x6f, 0x6c, 0x6c, 0x65, 0x72, 0x2f, 0x61, 0x70, 0x69,
 	0x2f, 0x76, 0x31, 0x2f, 0x65, 0x72, 0x72, 0x6f, 0x72, 0x2e, 0x70, 0x72, 0x6f, 0x74, 0x6f, 0x12,
 	0x11, 0x63, 0x6f, 0x6e, 0x74, 0x72, 0x6f, 0x6c, 0x6c, 0x65, 0x72, 0x2e, 0x61, 0x70, 0x69, 0x2e,
-	0x76, 0x31, 0x1a, 0x1e, 0x67, 0x6f, 0x6f, 0x67, 0x6c, 0x65, 0x2f, 0x70, 0x72, 0x6f, 0x74, 0x6f,
-	0x62, 0x75, 0x66, 0x2f, 0x77, 0x72, 0x61, 0x70, 0x70, 0x65, 0x72, 0x73, 0x2e, 0x70, 0x72, 0x6f,
-	0x74, 0x6f, 0x22, 0xad, 0x01, 0x0a, 0x0c, 0x45, 0x72, 0x72, 0x6f, 0x72, 0x44, 0x65, 0x74, 0x61,
-	0x69, 0x6c, 0x73, 0x12, 0x37, 0x0a, 0x08, 0x74, 0x72, 0x61, 0x63, 0x65, 0x5f, 0x69, 0x64, 0x18,
-	0x01, 0x20, 0x01, 0x28, 0x0b, 0x32, 0x1c, 0x2e, 0x67, 0x6f, 0x6f, 0x67, 0x6c, 0x65, 0x2e, 0x70,
-	0x72, 0x6f, 0x74, 0x6f, 0x62, 0x75, 0x66, 0x2e, 0x53, 0x74, 0x72, 0x69, 0x6e, 0x67, 0x56, 0x61,
-	0x6c, 0x75, 0x65, 0x52, 0x07, 0x54, 0x72, 0x61, 0x63, 0x65, 0x49, 0x64, 0x12, 0x3c, 0x0a, 0x0a,
-	0x72, 0x65, 0x71, 0x75, 0x65, 0x73, 0x74, 0x5f, 0x69, 0x64, 0x18, 0x02, 0x20, 0x01, 0x28, 0x0b,
-	0x32, 0x1c, 0x2e, 0x67, 0x6f, 0x6f, 0x67, 0x6c, 0x65, 0x2e, 0x70, 0x72, 0x6f, 0x74, 0x6f, 0x62,
-	0x75, 0x66, 0x2e, 0x53, 0x74, 0x72, 0x69, 0x6e, 0x67, 0x56, 0x61, 0x6c, 0x75, 0x65, 0x52, 0x0a,
-	0x72, 0x65, 0x71, 0x75, 0x65, 0x73, 0x74, 0x5f, 0x69, 0x64, 0x12, 0x26, 0x0a, 0x0e, 0x72, 0x65,
-	0x71, 0x75, 0x65, 0x73, 0x74, 0x5f, 0x66, 0x69, 0x65, 0x6c, 0x64, 0x73, 0x18, 0x03, 0x20, 0x03,
-	0x28, 0x09, 0x52, 0x0e, 0x72, 0x65, 0x71, 0x75, 0x65, 0x73, 0x74, 0x5f, 0x66, 0x69, 0x65, 0x6c,
-	0x64, 0x73, 0x22, 0xe1, 0x01, 0x0a, 0x05, 0x45, 0x72, 0x72, 0x6f, 0x72, 0x12, 0x33, 0x0a, 0x06,
-	0x73, 0x74, 0x61, 0x74, 0x75, 0x73, 0x18, 0x01, 0x20, 0x01, 0x28, 0x0b, 0x32, 0x1b, 0x2e, 0x67,
-	0x6f, 0x6f, 0x67, 0x6c, 0x65, 0x2e, 0x70, 0x72, 0x6f, 0x74, 0x6f, 0x62, 0x75, 0x66, 0x2e, 0x49,
-	0x6e, 0x74, 0x36, 0x34, 0x56, 0x61, 0x6c, 0x75, 0x65, 0x52, 0x06, 0x73, 0x74, 0x61, 0x74, 0x75,
-	0x73, 0x12, 0x30, 0x0a, 0x04, 0x63, 0x6f, 0x64, 0x65, 0x18, 0x02, 0x20, 0x01, 0x28, 0x0b, 0x32,
-	0x1c, 0x2e, 0x67, 0x6f, 0x6f, 0x67, 0x6c, 0x65, 0x2e, 0x70, 0x72, 0x6f, 0x74, 0x6f, 0x62, 0x75,
-	0x66, 0x2e, 0x53, 0x74, 0x72, 0x69, 0x6e, 0x67, 0x56, 0x61, 0x6c, 0x75, 0x65, 0x52, 0x04, 0x63,
-	0x6f, 0x64, 0x65, 0x12, 0x36, 0x0a, 0x07, 0x6d, 0x65, 0x73, 0x73, 0x61, 0x67, 0x65, 0x18, 0x03,
-	0x20, 0x01, 0x28, 0x0b, 0x32, 0x1c, 0x2e, 0x67, 0x6f, 0x6f, 0x67, 0x6c, 0x65, 0x2e, 0x70, 0x72,
-	0x6f, 0x74, 0x6f, 0x62, 0x75, 0x66, 0x2e, 0x53, 0x74, 0x72, 0x69, 0x6e, 0x67, 0x56, 0x61, 0x6c,
-	0x75, 0x65, 0x52, 0x07, 0x6d, 0x65, 0x73, 0x73, 0x61, 0x67, 0x65, 0x12, 0x39, 0x0a, 0x07, 0x64,
-	0x65, 0x74, 0x61, 0x69, 0x6c, 0x73, 0x18, 0x04, 0x20, 0x01, 0x28, 0x0b, 0x32, 0x1f, 0x2e, 0x63,
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-	0x72, 0x2f, 0x61, 0x70, 0x69, 0x3b, 0x61, 0x70, 0x69, 0x62, 0x06, 0x70, 0x72, 0x6f, 0x74, 0x6f,
-	0x33,
+	0x76, 0x31, 0x22, 0x70, 0x0a, 0x0c, 0x45, 0x72, 0x72, 0x6f, 0x72, 0x44, 0x65, 0x74, 0x61, 0x69,
+	0x6c, 0x73, 0x12, 0x18, 0x0a, 0x07, 0x54, 0x72, 0x61, 0x63, 0x65, 0x49, 0x64, 0x18, 0x01, 0x20,
+	0x01, 0x28, 0x09, 0x52, 0x07, 0x54, 0x72, 0x61, 0x63, 0x65, 0x49, 0x64, 0x12, 0x1e, 0x0a, 0x0a,
+	0x72, 0x65, 0x71, 0x75, 0x65, 0x73, 0x74, 0x5f, 0x69, 0x64, 0x18, 0x02, 0x20, 0x01, 0x28, 0x09,
+	0x52, 0x0a, 0x72, 0x65, 0x71, 0x75, 0x65, 0x73, 0x74, 0x5f, 0x69, 0x64, 0x12, 0x26, 0x0a, 0x0e,
+	0x72, 0x65, 0x71, 0x75, 0x65, 0x73, 0x74, 0x5f, 0x66, 0x69, 0x65, 0x6c, 0x64, 0x73, 0x18, 0x03,
+	0x20, 0x03, 0x28, 0x09, 0x52, 0x0e, 0x72, 0x65, 0x71, 0x75, 0x65, 0x73, 0x74, 0x5f, 0x66, 0x69,
+	0x65, 0x6c, 0x64, 0x73, 0x22, 0x88, 0x01, 0x0a, 0x05, 0x45, 0x72, 0x72, 0x6f, 0x72, 0x12, 0x16,
+	0x0a, 0x06, 0x73, 0x74, 0x61, 0x74, 0x75, 0x73, 0x18, 0x01, 0x20, 0x01, 0x28, 0x05, 0x52, 0x06,
+	0x73, 0x74, 0x61, 0x74, 0x75, 0x73, 0x12, 0x12, 0x0a, 0x04, 0x63, 0x6f, 0x64, 0x65, 0x18, 0x02,
+	0x20, 0x01, 0x28, 0x09, 0x52, 0x04, 0x63, 0x6f, 0x64, 0x65, 0x12, 0x18, 0x0a, 0x07, 0x6d, 0x65,
+	0x73, 0x73, 0x61, 0x67, 0x65, 0x18, 0x03, 0x20, 0x01, 0x28, 0x09, 0x52, 0x07, 0x6d, 0x65, 0x73,
+	0x73, 0x61, 0x67, 0x65, 0x12, 0x39, 0x0a, 0x07, 0x64, 0x65, 0x74, 0x61, 0x69, 0x6c, 0x73, 0x18,
+	0x04, 0x20, 0x01, 0x28, 0x0b, 0x32, 0x1f, 0x2e, 0x63, 0x6f, 0x6e, 0x74, 0x72, 0x6f, 0x6c, 0x6c,
+	0x65, 0x72, 0x2e, 0x61, 0x70, 0x69, 0x2e, 0x76, 0x31, 0x2e, 0x45, 0x72, 0x72, 0x6f, 0x72, 0x44,
+	0x65, 0x74, 0x61, 0x69, 0x6c, 0x73, 0x52, 0x07, 0x64, 0x65, 0x74, 0x61, 0x69, 0x6c, 0x73, 0x42,
+	0x41, 0x5a, 0x3f, 0x67, 0x69, 0x74, 0x68, 0x75, 0x62, 0x2e, 0x63, 0x6f, 0x6d, 0x2f, 0x68, 0x61,
+	0x73, 0x68, 0x69, 0x63, 0x6f, 0x72, 0x70, 0x2f, 0x77, 0x61, 0x74, 0x63, 0x68, 0x74, 0x6f, 0x77,
+	0x65, 0x72, 0x2f, 0x69, 0x6e, 0x74, 0x65, 0x72, 0x6e, 0x61, 0x6c, 0x2f, 0x67, 0x65, 0x6e, 0x2f,
+	0x63, 0x6f, 0x6e, 0x74, 0x72, 0x6f, 0x6c, 0x6c, 0x65, 0x72, 0x2f, 0x61, 0x70, 0x69, 0x3b, 0x61,
+	0x70, 0x69, 0x62, 0x06, 0x70, 0x72, 0x6f, 0x74, 0x6f, 0x33,
 }
 
 var (
@@ -221,23 +208,16 @@ func file_controller_api_v1_error_proto_rawDescGZIP() []byte {
 
 var file_controller_api_v1_error_proto_msgTypes = make([]protoimpl.MessageInfo, 2)
 var file_controller_api_v1_error_proto_goTypes = []interface{}{
-	(*ErrorDetails)(nil),         // 0: controller.api.v1.ErrorDetails
-	(*Error)(nil),                // 1: controller.api.v1.Error
-	(*wrappers.StringValue)(nil), // 2: google.protobuf.StringValue
-	(*wrappers.Int64Value)(nil),  // 3: google.protobuf.Int64Value
+	(*ErrorDetails)(nil), // 0: controller.api.v1.ErrorDetails
+	(*Error)(nil),        // 1: controller.api.v1.Error
 }
 var file_controller_api_v1_error_proto_depIdxs = []int32{
-	2, // 0: controller.api.v1.ErrorDetails.trace_id:type_name -> google.protobuf.StringValue
-	2, // 1: controller.api.v1.ErrorDetails.request_id:type_name -> google.protobuf.StringValue
-	3, // 2: controller.api.v1.Error.status:type_name -> google.protobuf.Int64Value
-	2, // 3: controller.api.v1.Error.code:type_name -> google.protobuf.StringValue
-	2, // 4: controller.api.v1.Error.message:type_name -> google.protobuf.StringValue
-	0, // 5: controller.api.v1.Error.details:type_name -> controller.api.v1.ErrorDetails
-	6, // [6:6] is the sub-list for method output_type
-	6, // [6:6] is the sub-list for method input_type
-	6, // [6:6] is the sub-list for extension type_name
-	6, // [6:6] is the sub-list for extension extendee
-	0, // [0:6] is the sub-list for field type_name
+	0, // 0: controller.api.v1.Error.details:type_name -> controller.api.v1.ErrorDetails
+	1, // [1:1] is the sub-list for method output_type
+	1, // [1:1] is the sub-list for method input_type
+	1, // [1:1] is the sub-list for extension type_name
+	1, // [1:1] is the sub-list for extension extendee
+	0, // [0:1] is the sub-list for field type_name
 }
 
 func init() { file_controller_api_v1_error_proto_init() }
diff --git a/internal/proto/local/controller/api/v1/error.proto b/internal/proto/local/controller/api/v1/error.proto
index c4eb2f5a43..1046011459 100644
--- a/internal/proto/local/controller/api/v1/error.proto
+++ b/internal/proto/local/controller/api/v1/error.proto
@@ -4,22 +4,20 @@ package controller.api.v1;
 
 option go_package = "github.com/hashicorp/watchtower/internal/gen/controller/api;api";
 
-import "google/protobuf/wrappers.proto";
-
 message ErrorDetails {
-	google.protobuf.StringValue trace_id = 1 [json_name="TraceId"];
-	google.protobuf.StringValue request_id = 2 [json_name="request_id"];
+	string TraceId = 1 [json_name="TraceId"];
+	string request_id = 2 [json_name="request_id"];
 	repeated string request_fields = 3 [json_name="request_fields"];
 }
 
 // Error is returned by the JSON API when an error occurs.
 message Error {
 	// The HTTP Status code applicable to this error
-	google.protobuf.Int64Value status = 1;
+	int32 status = 1;
 	// An application-specific error string
-	google.protobuf.StringValue code = 2;
+	string code = 2;
 	// A human readable explanation specific to this occurrence of the error
-	google.protobuf.StringValue message = 3;
+	string message = 3;
 	// Additional metadata regarding the error. Depending on the error
 	// different fields will be populated.
 	ErrorDetails details = 4;
diff --git a/internal/servers/controller/handler.go b/internal/servers/controller/handler.go
index 8998c1f474..980c9661e1 100644
--- a/internal/servers/controller/handler.go
+++ b/internal/servers/controller/handler.go
@@ -15,6 +15,7 @@ import (
 	"github.com/hashicorp/watchtower/api"
 	"github.com/hashicorp/watchtower/globals"
 	"github.com/hashicorp/watchtower/internal/gen/controller/api/services"
+	"github.com/hashicorp/watchtower/internal/servers/controller/handlers"
 	"github.com/hashicorp/watchtower/internal/servers/controller/handlers/host_catalogs"
 	"github.com/hashicorp/watchtower/internal/servers/controller/handlers/host_sets"
 	"github.com/hashicorp/watchtower/internal/servers/controller/handlers/hosts"
@@ -57,7 +58,7 @@ func handleGrpcGateway(c *Controller) http.Handler {
 	// Register*ServiceHandlerServer methods ignore the passed in ctx.  Using the baseContext now just in case this changes
 	// in the future, at which point we'll want to be using the baseContext.
 	ctx := c.baseContext
-	mux := runtime.NewServeMux()
+	mux := runtime.NewServeMux(runtime.WithProtoErrorHandler(handlers.ErrorHandler(c.logger)))
 	services.RegisterHostCatalogServiceHandlerServer(ctx, mux, &host_catalogs.Service{})
 	services.RegisterHostSetServiceHandlerServer(ctx, mux, &host_sets.Service{})
 	services.RegisterHostServiceHandlerServer(ctx, mux, &hosts.Service{})
diff --git a/internal/servers/controller/handlers/errors.go b/internal/servers/controller/handlers/errors.go
new file mode 100644
index 0000000000..cf4219d750
--- /dev/null
+++ b/internal/servers/controller/handlers/errors.go
@@ -0,0 +1,88 @@
+package handlers
+
+import (
+	"context"
+	"fmt"
+	"io"
+	"net/http"
+
+	"github.com/grpc-ecosystem/grpc-gateway/runtime"
+	"github.com/hashicorp/go-hclog"
+	pb "github.com/hashicorp/watchtower/internal/gen/controller/api"
+	"google.golang.org/genproto/googleapis/rpc/errdetails"
+	"google.golang.org/grpc/codes"
+	"google.golang.org/grpc/status"
+)
+
+func NotFoundErrorf(msg string, a ...interface{}) error {
+	return status.Errorf(codes.NotFound, msg, a...)
+}
+
+func InvalidArgumentErrorf(msg string, fields []string) error {
+	st := status.New(codes.InvalidArgument, msg)
+	br := &errdetails.BadRequest{}
+	for _, f := range fields {
+		br.FieldViolations = append(br.FieldViolations, &errdetails.BadRequest_FieldViolation{Field: f})
+	}
+	st, err := st.WithDetails(br)
+	if err != nil {
+		hclog.Default().Error("failure building status with details", "details", br, "error", err)
+		return status.Error(codes.Internal, "Failed to build InvalidArgument error.")
+	}
+	return st.Err()
+}
+
+func statusErrorToApiError(s *status.Status) *pb.Error {
+	apiErr := &pb.Error{}
+	apiErr.Status = int32(runtime.HTTPStatusFromCode(s.Code()))
+	apiErr.Message = s.Message()
+	// TODO(ICU-193): Decouple from the status codes and instead use codes defined specifically for our API.
+	apiErr.Code = s.Code().String()
+
+	for _, ed := range s.Details() {
+		switch ed.(type) {
+		case *errdetails.BadRequest:
+			br := ed.(*errdetails.BadRequest)
+			for _, fv := range br.GetFieldViolations() {
+				if apiErr.Details == nil {
+					apiErr.Details = &pb.ErrorDetails{}
+				}
+				apiErr.Details.RequestFields = append(apiErr.Details.RequestFields, fv.GetField())
+			}
+		}
+	}
+	return apiErr
+}
+
+// TODO(ICU-194): Remove all information from internal errors.
+func ErrorHandler(logger hclog.Logger) runtime.ProtoErrorHandlerFunc {
+	const errorFallback = `{"error": "failed to marshal error message"}`
+	return func(ctx context.Context, _ *runtime.ServeMux, marshaler runtime.Marshaler, w http.ResponseWriter, r *http.Request, inErr error) {
+		if inErr == runtime.ErrUnknownURI {
+			// grpc gateway uses this error when the path was not matched, but the error uses codes.Unimplemented which doesn't match the intention.
+			// Overwrite the error to match our expected behavior.
+			inErr = status.Error(codes.NotFound, http.StatusText(http.StatusNotFound))
+		}
+		s, ok := status.FromError(inErr)
+		if !ok {
+			s = status.New(codes.Unknown, inErr.Error())
+		}
+		apiErr := statusErrorToApiError(s)
+		buf, merr := marshaler.Marshal(apiErr)
+		if merr != nil {
+			logger.Error("failed to marshal error response", "response", fmt.Sprintf("%#v", apiErr), "error", merr)
+			w.WriteHeader(http.StatusInternalServerError)
+			if _, err := io.WriteString(w, errorFallback); err != nil {
+				logger.Error("failed to write response", "error", err)
+			}
+			return
+		}
+
+		w.Header().Set("Content-Type", marshaler.ContentType())
+		w.WriteHeader(int(apiErr.GetStatus()))
+		if _, err := w.Write(buf); err != nil {
+			logger.Error("failed to send response chunk", "error", err)
+			return
+		}
+	}
+}
diff --git a/internal/servers/controller/handlers/errors_test.go b/internal/servers/controller/handlers/errors_test.go
new file mode 100644
index 0000000000..9eff9abab4
--- /dev/null
+++ b/internal/servers/controller/handlers/errors_test.go
@@ -0,0 +1,101 @@
+package handlers
+
+import (
+	"context"
+	"io/ioutil"
+	"net/http"
+	"net/http/httptest"
+	"testing"
+
+	"github.com/golang/protobuf/proto"
+	"github.com/grpc-ecosystem/grpc-gateway/runtime"
+	"github.com/hashicorp/go-hclog"
+	pb "github.com/hashicorp/watchtower/internal/gen/controller/api"
+	"github.com/stretchr/testify/assert"
+	sdpb "google.golang.org/genproto/googleapis/rpc/errdetails"
+	"google.golang.org/grpc/codes"
+	"google.golang.org/grpc/status"
+)
+
+func TestApiErrorHandler(t *testing.T) {
+	ctx := context.Background()
+	req, err := http.NewRequest("GET", "madeup/for/the/test", nil)
+	if err != nil {
+		t.Fatalf("Couldn't create test request")
+	}
+	mux := runtime.NewServeMux()
+	_, outMarsh := runtime.MarshalerForRequest(mux, req)
+
+	tested := ErrorHandler(hclog.L())
+
+	testCases := []struct {
+		name          string
+		err           error
+		statusDetails []proto.Message
+		expected      *pb.Error
+	}{
+		{
+			name: "Not Found",
+			err:  status.Error(codes.NotFound, "test"),
+			expected: &pb.Error{
+				Status:  404,
+				Code:    codes.NotFound.String(),
+				Message: "test",
+			},
+		},
+		{
+			name: "GrpcGateway Routing Error",
+			err:  runtime.ErrUnknownURI,
+			expected: &pb.Error{
+				Status:  404,
+				Code:    codes.NotFound.String(),
+				Message: http.StatusText(http.StatusNotFound),
+			},
+		},
+		{
+			name: "Invalid Fields",
+			err:  status.Error(codes.InvalidArgument, "test"),
+			statusDetails: []proto.Message{
+				&sdpb.BadRequest{
+					FieldViolations: []*sdpb.BadRequest_FieldViolation{
+						{Field: "first"},
+						{Field: "second"},
+					},
+				},
+			},
+			expected: &pb.Error{
+				Status:  400,
+				Code:    codes.InvalidArgument.String(),
+				Message: "test",
+				Details: &pb.ErrorDetails{
+					RequestFields: []string{"first", "second"},
+				},
+			},
+		},
+	}
+	for _, tc := range testCases {
+		t.Run(tc.name, func(t *testing.T) {
+			assert := assert.New(t)
+
+			if tc.statusDetails != nil {
+				s, ok := status.FromError(tc.err)
+				assert.True(ok)
+				s, err := s.WithDetails(tc.statusDetails...)
+				assert.NoError(err)
+				tc.err = s.Err()
+			}
+
+			w := httptest.NewRecorder()
+			tested(ctx, mux, outMarsh, w, req, tc.err)
+			resp := w.Result()
+			assert.EqualValues(tc.expected.Status, resp.StatusCode)
+
+			got, err := ioutil.ReadAll(resp.Body)
+			assert.NoError(err)
+			want, err := outMarsh.Marshal(tc.expected)
+			t.Logf("Got marshaled error: %q", want)
+			assert.NoError(err)
+			assert.JSONEq(string(want), string(got))
+		})
+	}
+}
diff --git a/internal/servers/controller/handlers/projects/project_service.go b/internal/servers/controller/handlers/projects/project_service.go
index 8fe01e2faa..eb409765df 100644
--- a/internal/servers/controller/handlers/projects/project_service.go
+++ b/internal/servers/controller/handlers/projects/project_service.go
@@ -11,6 +11,7 @@ import (
 	pb "github.com/hashicorp/watchtower/internal/gen/controller/api/resources/scopes"
 	pbs "github.com/hashicorp/watchtower/internal/gen/controller/api/services"
 	"github.com/hashicorp/watchtower/internal/iam"
+	"github.com/hashicorp/watchtower/internal/servers/controller/handlers"
 	"google.golang.org/grpc/codes"
 	"google.golang.org/grpc/status"
 )
@@ -97,7 +98,7 @@ func (s Service) getFromRepo(ctx context.Context, id string) (*pb.Project, error
 		return nil, err
 	}
 	if p == nil {
-		return nil, status.Errorf(codes.NotFound, "Could not find Project with id %q", id)
+		return nil, handlers.NotFoundErrorf("Project %q doesn't exist.", id)
 	}
 	return toProto(p), nil
 }
@@ -112,20 +113,20 @@ func (s Service) createInRepo(ctx context.Context, orgID string, item *pb.Projec
 	}
 	p, err := iam.NewProject(orgID, opts...)
 	if err != nil {
-		return nil, err
+		return nil, status.Errorf(codes.Internal, "Unable to build project for creation: %v.", err)
 	}
 	out, err := s.repo.CreateScope(ctx, p)
 	if err != nil {
-		return nil, err
+		return nil, status.Errorf(codes.Internal, "Unable to create project: %v.", err)
 	}
 	if out == nil {
-		return nil, status.Error(codes.Internal, "Unable to create scope but no error returned from repository.")
+		return nil, status.Error(codes.Internal, "Unable to create project but no error returned from repository.")
 	}
 	return toProto(out), nil
 }
 
-func (s Service) updateInRepo(ctx context.Context, orgID, projID string, mask []string, item *pb.Project) (*pb.Project, error) {
-	opts := []iam.Option{iam.WithPublicId(projID)}
+func (s Service) updateInRepo(ctx context.Context, orgID, projId string, mask []string, item *pb.Project) (*pb.Project, error) {
+	opts := []iam.Option{iam.WithPublicId(projId)}
 	if desc := item.GetDescription(); desc != nil {
 		opts = append(opts, iam.WithDescription(desc.GetValue()))
 	}
@@ -134,21 +135,21 @@ func (s Service) updateInRepo(ctx context.Context, orgID, projID string, mask []
 	}
 	p, err := iam.NewProject(orgID, opts...)
 	if err != nil {
-		return nil, err
+		return nil, status.Errorf(codes.Internal, "Unable to build project for update: %v.", err)
 	}
 	dbMask, err := toDbUpdateMask(mask)
 	if err != nil {
 		return nil, err
 	}
 	if len(dbMask) == 0 {
-		return nil, status.Errorf(codes.InvalidArgument, "No valid fields included in the update mask.")
+		return nil, handlers.InvalidArgumentErrorf("No valid fields included in the update mask.", []string{"update_mask"})
 	}
-	out, _, err := s.repo.UpdateScope(ctx, p, dbMask)
+	out, rowsUpdated, err := s.repo.UpdateScope(ctx, p, dbMask)
 	if err != nil {
-		return nil, err
+		return nil, status.Errorf(codes.Internal, "Unable to update project: %v.", err)
 	}
-	if out == nil {
-		return nil, status.Error(codes.NotFound, "Project doesn't exist.")
+	if rowsUpdated == 0 {
+		return nil, handlers.NotFoundErrorf("Project %q doesn't exist.", projId)
 	}
 	return toProto(out), nil
 }
@@ -156,7 +157,7 @@ func (s Service) updateInRepo(ctx context.Context, orgID, projID string, mask []
 func (s Service) deleteFromRepo(ctx context.Context, projId string) (bool, error) {
 	rows, err := s.repo.DeleteScope(ctx, projId)
 	if err != nil {
-		return false, status.Errorf(codes.Internal, "Unable to delete project: %v", err)
+		return false, status.Errorf(codes.Internal, "Unable to delete project: %v.", err)
 	}
 	return rows > 0, nil
 }
@@ -175,7 +176,7 @@ func toDbUpdateMask(paths []string) ([]string, error) {
 		}
 	}
 	if len(invalid) > 0 {
-		return nil, status.Errorf(codes.InvalidArgument, "Invalid fields passed in update_update mask: %v", invalid)
+		return nil, handlers.InvalidArgumentErrorf(fmt.Sprintf("Invalid fields passed in update_update mask: %v.", invalid), []string{"update_mask"})
 	}
 	return dbPaths, nil
 }
@@ -203,11 +204,15 @@ func validateGetProjectRequest(req *pbs.GetProjectRequest) error {
 	if err := validateAncestors(req); err != nil {
 		return err
 	}
-	if err := validateID(req.GetOrgId(), "o_"); err != nil {
-		return err
+	badFormat := []string{}
+	if !validID(req.GetId(), "p_") {
+		badFormat = append(badFormat, "id")
 	}
-	if err := validateID(req.GetId(), "p_"); err != nil {
-		return err
+	if !validID(req.GetOrgId(), "o_") {
+		badFormat = append(badFormat, "id")
+	}
+	if len(badFormat) > 0 {
+		return handlers.InvalidArgumentErrorf("Improperly formatted identifier.", badFormat)
 	}
 	return nil
 }
@@ -216,18 +221,25 @@ func validateCreateProjectRequest(req *pbs.CreateProjectRequest) error {
 	if err := validateAncestors(req); err != nil {
 		return err
 	}
-	if err := validateID(req.GetOrgId(), "o_"); err != nil {
-		return err
+	if !validID(req.GetOrgId(), "o_") {
+		handlers.InvalidArgumentErrorf("Improperly formatted identifier.", []string{"org_id"})
 	}
 	item := req.GetItem()
 	if item == nil {
-		return status.Errorf(codes.InvalidArgument, "A project's fields must be set to something .")
+		return handlers.InvalidArgumentErrorf("A project's fields must be set to something.", []string{"item"})
 	}
+	immutableFieldsSet := []string{}
 	if item.GetId() != "" {
-		return status.Errorf(codes.InvalidArgument, "Cannot set ID when creating a new project.")
+		immutableFieldsSet = append(immutableFieldsSet, "id")
+	}
+	if item.GetCreatedTime() != nil {
+		immutableFieldsSet = append(immutableFieldsSet, "created_time")
+	}
+	if item.GetUpdatedTime() != nil {
+		immutableFieldsSet = append(immutableFieldsSet, "updated_time")
 	}
-	if item.GetCreatedTime() != nil || item.GetUpdatedTime() != nil {
-		return status.Errorf(codes.InvalidArgument, "Cannot set Created or Updated time when creating a new project.")
+	if len(immutableFieldsSet) > 0 {
+		return handlers.InvalidArgumentErrorf("Cannot specify read only fields at creation time.", immutableFieldsSet)
 	}
 	return nil
 }
@@ -236,30 +248,42 @@ func validateUpdateProjectRequest(req *pbs.UpdateProjectRequest) error {
 	if err := validateAncestors(req); err != nil {
 		return err
 	}
-	if err := validateID(req.GetId(), "p_"); err != nil {
-		return err
+	badFormat := []string{}
+	if !validID(req.GetId(), "p_") {
+		badFormat = append(badFormat, "id")
 	}
-	if err := validateID(req.GetOrgId(), "o_"); err != nil {
-		return err
+	if !validID(req.GetOrgId(), "o_") {
+		badFormat = append(badFormat, "id")
+	}
+	if len(badFormat) > 0 {
+		handlers.InvalidArgumentErrorf("Improperly formatted identifier.", badFormat)
 	}
+
 	if req.GetUpdateMask() == nil {
-		return status.Errorf(codes.InvalidArgument, "UpdateMask not provided but is required to update a project.")
+		return handlers.InvalidArgumentErrorf("UpdateMask not provided but is required to update a project.", []string{"update_mask"})
 	}
+
 	item := req.GetItem()
 	if item == nil {
 		// It is legitimate for no item to be specified in an update request as it indicates all fields provided in
 		// the mask will be marked as unset.
 		return nil
 	}
-
-	if err := validateID(item.GetId(), "p_"); item.GetId() != "" && err != nil {
-		return err
-	}
 	if item.GetId() != "" && item.GetId() != req.GetId() {
-		return status.Errorf(codes.InvalidArgument, "Id in provided item and url must match. Item Id was %q, url id was %q", item.GetId(), req.GetId())
+		return handlers.InvalidArgumentErrorf("Id in provided item and url do not match.", []string{"id"})
+	}
+	immutableFieldsSet := []string{}
+	if item.GetId() != "" {
+		immutableFieldsSet = append(immutableFieldsSet, "id")
 	}
-	if item.GetCreatedTime() != nil || item.GetUpdatedTime() != nil {
-		return status.Errorf(codes.InvalidArgument, "Cannot set Created or Updated time when updating a project.")
+	if item.GetCreatedTime() != nil {
+		immutableFieldsSet = append(immutableFieldsSet, "created_time")
+	}
+	if item.GetUpdatedTime() != nil {
+		immutableFieldsSet = append(immutableFieldsSet, "updated_time")
+	}
+	if len(immutableFieldsSet) > 0 {
+		return handlers.InvalidArgumentErrorf("Cannot specify read only fields at update time.", immutableFieldsSet)
 	}
 
 	return nil
@@ -269,24 +293,28 @@ func validateDeleteProjectRequest(req *pbs.DeleteProjectRequest) error {
 	if err := validateAncestors(req); err != nil {
 		return err
 	}
-	if err := validateID(req.GetId(), "p_"); err != nil {
-		return err
+	badFields := []string{}
+	if !validID(req.GetId(), "p_") {
+		badFields = append(badFields, "id")
 	}
-	if err := validateID(req.GetOrgId(), "o_"); err != nil {
-		return err
+	if !validID(req.GetOrgId(), "o_") {
+		badFields = append(badFields, "org_id")
+	}
+	if len(badFields) > 0 {
+		return handlers.InvalidArgumentErrorf("Improperly formatted id.", badFields)
 	}
 	return nil
 }
 
-func validateID(id, prefix string) error {
+func validID(id, prefix string) bool {
 	if !strings.HasPrefix(id, prefix) {
-		return status.Errorf(codes.InvalidArgument, "ID start with a %q prefix, provided %q", prefix, id)
+		return false
 	}
 	id = strings.TrimPrefix(id, prefix)
 	if reInvalidID.Match([]byte(id)) {
-		return status.Errorf(codes.InvalidArgument, "Improperly formatted ID: %q", id)
+		return false
 	}
-	return nil
+	return true
 }
 
 type ancestorProvider interface {
@@ -296,7 +324,7 @@ type ancestorProvider interface {
 // validateAncestors verifies that the ancestors of this call are properly set and provided.
 func validateAncestors(r ancestorProvider) error {
 	if r.GetOrgId() == "" {
-		return status.Errorf(codes.InvalidArgument, "org_id must be provided.")
+		return handlers.InvalidArgumentErrorf("Missing organization id.", []string{"org_id"})
 	}
 	return nil
 }
diff --git a/internal/servers/controller/handlers/projects/service_test.go b/internal/servers/controller/handlers/projects/service_test.go
index 8d25ac1183..8559864eeb 100644
--- a/internal/servers/controller/handlers/projects/service_test.go
+++ b/internal/servers/controller/handlers/projects/service_test.go
@@ -470,6 +470,8 @@ func TestUpdate(t *testing.T) {
 			},
 			errCode: codes.OK,
 		},
+		// TODO: Updating a non existant project should result in a NotFound exception but currently results in
+		// the repo returning an internal error.
 		{
 			name: "Update a Non Existing Project",
 			req: &pbs.UpdateProjectRequest{
@@ -482,7 +484,7 @@ func TestUpdate(t *testing.T) {
 					Description: &wrappers.StringValue{Value: "desc"},
 				},
 			},
-			errCode: codes.Unknown,
+			errCode: codes.Internal,
 		},
 		{
 			name: "Cant change Id",