diff --git a/api/server/httputils/httputils.go b/api/server/httputils/httputils.go
index 1d671693f6..386695ca32 100644
--- a/api/server/httputils/httputils.go
+++ b/api/server/httputils/httputils.go
@@ -2,6 +2,7 @@ package httputils // import "github.com/docker/docker/api/server/httputils"
 
 import (
 	"context"
+	"encoding/json"
 	"io"
 	"mime"
 	"net/http"
@@ -56,6 +57,35 @@ func CheckForJSON(r *http.Request) error {
 	return matchesContentType(ct, "application/json")
 }
 
+// ReadJSON validates the request to have the correct content-type, and decodes
+// the request's Body into out.
+func ReadJSON(r *http.Request, out interface{}) error {
+	err := CheckForJSON(r)
+	if err != nil {
+		return err
+	}
+	if r.Body == nil || r.ContentLength == 0 {
+		// an empty body is not invalid, so don't return an error; see
+		// https://lists.w3.org/Archives/Public/ietf-http-wg/2010JulSep/0272.html
+		return nil
+	}
+
+	dec := json.NewDecoder(r.Body)
+	err = dec.Decode(out)
+	defer r.Body.Close()
+	if err != nil {
+		if err == io.EOF {
+			return errdefs.InvalidParameter(errors.New("invalid JSON: got EOF while reading request body"))
+		}
+		return errdefs.InvalidParameter(errors.Wrap(err, "invalid JSON"))
+	}
+
+	if dec.More() {
+		return errdefs.InvalidParameter(errors.New("unexpected content after JSON"))
+	}
+	return nil
+}
+
 // ParseForm ensures the request form is parsed even with invalid content types.
 // If we don't do this, POST method without Content-type (even with empty body) will fail.
 func ParseForm(r *http.Request) error {
diff --git a/api/server/httputils/httputils_test.go b/api/server/httputils/httputils_test.go
index 81602c0836..6f796feede 100644
--- a/api/server/httputils/httputils_test.go
+++ b/api/server/httputils/httputils_test.go
@@ -1,6 +1,10 @@
 package httputils // import "github.com/docker/docker/api/server/httputils"
 
-import "testing"
+import (
+	"net/http"
+	"strings"
+	"testing"
+)
 
 // matchesContentType
 func TestJsonContentType(t *testing.T) {
@@ -26,3 +30,101 @@ func TestJsonContentType(t *testing.T) {
 		t.Errorf(`expected "%s", got "%v"`, expected, err)
 	}
 }
+
+func TestReadJSON(t *testing.T) {
+	t.Run("nil body", func(t *testing.T) {
+		req, err := http.NewRequest("POST", "https://example.com/some/path", nil)
+		if err != nil {
+			t.Error(err)
+		}
+		foo := struct{}{}
+		err = ReadJSON(req, &foo)
+		if err != nil {
+			t.Error(err)
+		}
+	})
+
+	t.Run("empty body", func(t *testing.T) {
+		req, err := http.NewRequest("POST", "https://example.com/some/path", strings.NewReader(""))
+		if err != nil {
+			t.Error(err)
+		}
+		foo := struct{ SomeField string }{}
+		err = ReadJSON(req, &foo)
+		if err != nil {
+			t.Error(err)
+		}
+		if foo.SomeField != "" {
+			t.Errorf("expected: '', got: %s", foo.SomeField)
+		}
+	})
+
+	t.Run("with valid request", func(t *testing.T) {
+		req, err := http.NewRequest("POST", "https://example.com/some/path", strings.NewReader(`{"SomeField":"some value"}`))
+		if err != nil {
+			t.Error(err)
+		}
+		req.Header.Set("Content-Type", "application/json")
+		foo := struct{ SomeField string }{}
+		err = ReadJSON(req, &foo)
+		if err != nil {
+			t.Error(err)
+		}
+		if foo.SomeField != "some value" {
+			t.Errorf("expected: 'some value', got: %s", foo.SomeField)
+		}
+	})
+	t.Run("with whitespace", func(t *testing.T) {
+		req, err := http.NewRequest("POST", "https://example.com/some/path", strings.NewReader(`
+
+	{"SomeField":"some value"}
+
+`))
+		if err != nil {
+			t.Error(err)
+		}
+		req.Header.Set("Content-Type", "application/json")
+		foo := struct{ SomeField string }{}
+		err = ReadJSON(req, &foo)
+		if err != nil {
+			t.Error(err)
+		}
+		if foo.SomeField != "some value" {
+			t.Errorf("expected: 'some value', got: %s", foo.SomeField)
+		}
+	})
+
+	t.Run("with extra content", func(t *testing.T) {
+		req, err := http.NewRequest("POST", "https://example.com/some/path", strings.NewReader(`{"SomeField":"some value"} and more content`))
+		if err != nil {
+			t.Error(err)
+		}
+		req.Header.Set("Content-Type", "application/json")
+		foo := struct{ SomeField string }{}
+		err = ReadJSON(req, &foo)
+		if err == nil {
+			t.Error("expected an error, got none")
+		}
+		expected := "unexpected content after JSON"
+		if err.Error() != expected {
+			t.Errorf("expected: '%s', got: %s", expected, err.Error())
+		}
+	})
+
+	t.Run("invalid JSON", func(t *testing.T) {
+		req, err := http.NewRequest("POST", "https://example.com/some/path", strings.NewReader(`{invalid json`))
+		if err != nil {
+			t.Error(err)
+		}
+		req.Header.Set("Content-Type", "application/json")
+		foo := struct{ SomeField string }{}
+		err = ReadJSON(req, &foo)
+		if err == nil {
+			t.Error("expected an error, got none")
+		}
+		expected := "invalid JSON: invalid character 'i' looking for beginning of object key string"
+		if err.Error() != expected {
+			t.Errorf("expected: '%s', got: %s", expected, err.Error())
+		}
+	})
+}
diff --git a/api/server/router/checkpoint/checkpoint_routes.go b/api/server/router/checkpoint/checkpoint_routes.go
index 6c03f976e2..678497b2a3 100644
--- a/api/server/router/checkpoint/checkpoint_routes.go
+++ b/api/server/router/checkpoint/checkpoint_routes.go
@@ -2,7 +2,6 @@ package checkpoint // import "github.com/docker/docker/api/server/router/checkpo
 
 import (
 	"context"
-	"encoding/json"
 	"net/http"
 
 	"github.com/docker/docker/api/server/httputils"
@@ -15,9 +14,7 @@ func (s *checkpointRouter) postContainerCheckpoint(ctx context.Context, w http.R
 	}
 
 	var options types.CheckpointCreateOptions
-
-	decoder := json.NewDecoder(r.Body)
-	if err := decoder.Decode(&options); err != nil {
+	if err := httputils.ReadJSON(r, &options); err != nil {
 		return err
 	}
 
diff --git a/api/server/router/container/container.go b/api/server/router/container/container.go
index df68fcb791..7ac9dc7aac 100644
--- a/api/server/router/container/container.go
+++ b/api/server/router/container/container.go
@@ -56,7 +56,7 @@ func (r *containerRouter) initRoutes() {
 		router.NewPostRoute("/containers/{name:.*}/wait", r.postContainersWait),
 		router.NewPostRoute("/containers/{name:.*}/resize", r.postContainersResize),
 		router.NewPostRoute("/containers/{name:.*}/attach", r.postContainersAttach),
-		router.NewPostRoute("/containers/{name:.*}/copy", r.postContainersCopy), // Deprecated since 1.8, Errors out since 1.12
+		router.NewPostRoute("/containers/{name:.*}/copy", r.postContainersCopy), // Deprecated since 1.8 (API v1.20), errors out since 1.12 (API v1.24)
 		router.NewPostRoute("/containers/{name:.*}/exec", r.postContainerExecCreate),
 		router.NewPostRoute("/exec/{name:.*}/start", r.postContainerExecStart),
 		router.NewPostRoute("/exec/{name:.*}/resize", r.postContainerExecResize),
diff --git a/api/server/router/container/container_routes.go b/api/server/router/container/container_routes.go
index de0a4474a7..392efc023e 100644
--- a/api/server/router/container/container_routes.go
+++ b/api/server/router/container/container_routes.go
@@ -427,14 +427,9 @@ func (s *containerRouter) postContainerUpdate(ctx context.Context, w http.Respon
 	if err := httputils.ParseForm(r); err != nil {
 		return err
 	}
-	if err := httputils.CheckForJSON(r); err != nil {
-		return err
-	}
 
 	var updateConfig container.UpdateConfig
-
-	decoder := json.NewDecoder(r.Body)
-	if err := decoder.Decode(&updateConfig); err != nil {
+	if err := httputils.ReadJSON(r, &updateConfig); err != nil {
 		return err
 	}
 	if versions.LessThan(httputils.VersionFromContext(ctx), "1.40") {
diff --git a/api/server/router/container/copy.go b/api/server/router/container/copy.go
index 47de35a455..28920b6d7b 100644
--- a/api/server/router/container/copy.go
+++ b/api/server/router/container/copy.go
@@ -6,14 +6,12 @@ import (
 	"context"
 	"encoding/base64"
 	"encoding/json"
-	"errors"
 	"io"
 	"net/http"
 
 	"github.com/docker/docker/api/server/httputils"
 	"github.com/docker/docker/api/types"
 	"github.com/docker/docker/api/types/versions"
-	"github.com/docker/docker/errdefs"
 	gddohttputil "github.com/golang/gddo/httputil"
 )
 
@@ -26,23 +24,18 @@ func (pathError) Error() string {
 func (pathError) InvalidParameter() {}
 
 // postContainersCopy is deprecated in favor of getContainersArchive.
+//
+// Deprecated since 1.8 (API v1.20), errors out since 1.12 (API v1.24)
 func (s *containerRouter) postContainersCopy(ctx context.Context, w http.ResponseWriter, r *http.Request, vars map[string]string) error {
-	// Deprecated since 1.8, Errors out since 1.12
 	version := httputils.VersionFromContext(ctx)
 	if versions.GreaterThanOrEqualTo(version, "1.24") {
 		w.WriteHeader(http.StatusNotFound)
 		return nil
 	}
-	if err := httputils.CheckForJSON(r); err != nil {
-		return err
-	}
 
 	cfg := types.CopyConfig{}
-	if err := json.NewDecoder(r.Body).Decode(&cfg); err != nil {
-		if err == io.EOF {
-			return errdefs.InvalidParameter(errors.New("got EOF while reading request body"))
-		}
-		return errdefs.InvalidParameter(err)
+	if err := httputils.ReadJSON(r, &cfg); err != nil {
+		return err
 	}
 
 	if cfg.Resource == "" {
diff --git a/api/server/router/container/exec.go b/api/server/router/container/exec.go
index cf92be1d2b..5a612bc977 100644
--- a/api/server/router/container/exec.go
+++ b/api/server/router/container/exec.go
@@ -2,8 +2,6 @@ package container // import "github.com/docker/docker/api/server/router/containe
 
 import (
 	"context"
-	"encoding/json"
-	"errors"
 	"fmt"
 	"io"
 	"net/http"
@@ -38,17 +36,10 @@ func (s *containerRouter) postContainerExecCreate(ctx context.Context, w http.Re
 	if err := httputils.ParseForm(r); err != nil {
 		return err
 	}
-	if err := httputils.CheckForJSON(r); err != nil {
-		return err
-	}
-	name := vars["name"]
 
 	execConfig := &types.ExecConfig{}
-	if err := json.NewDecoder(r.Body).Decode(execConfig); err != nil {
-		if err == io.EOF {
-			return errdefs.InvalidParameter(errors.New("got EOF while reading request body"))
-		}
-		return errdefs.InvalidParameter(err)
+	if err := httputils.ReadJSON(r, execConfig); err != nil {
+		return err
 	}
 
 	if len(execConfig.Cmd) == 0 {
@@ -56,9 +47,9 @@ func (s *containerRouter) postContainerExecCreate(ctx context.Context, w http.Re
 	}
 
 	// Register an instance of Exec in container.
-	id, err := s.backend.ContainerExecCreate(name, execConfig)
+	id, err := s.backend.ContainerExecCreate(vars["name"], execConfig)
 	if err != nil {
-		logrus.Errorf("Error setting up exec command in container %s: %v", name, err)
+		logrus.Errorf("Error setting up exec command in container %s: %v", vars["name"], err)
 		return err
 	}
 
@@ -74,9 +65,11 @@ func (s *containerRouter) postContainerExecStart(ctx context.Context, w http.Res
 	}
 
 	version := httputils.VersionFromContext(ctx)
-	if versions.GreaterThan(version, "1.21") {
-		if err := httputils.CheckForJSON(r); err != nil {
-			return err
+	if versions.LessThan(version, "1.22") {
+		// API versions before 1.22 did not enforce application/json content-type.
+		// Allow older clients to work by patching the content-type.
+		if r.Header.Get("Content-Type") != "application/json" {
+			r.Header.Set("Content-Type", "application/json")
 		}
 	}
 
@@ -87,11 +80,8 @@ func (s *containerRouter) postContainerExecStart(ctx context.Context, w http.Res
 	)
 
 	execStartCheck := &types.ExecStartCheck{}
-	if err := json.NewDecoder(r.Body).Decode(execStartCheck); err != nil {
-		if err == io.EOF {
-			return errdefs.InvalidParameter(errors.New("got EOF while reading request body"))
-		}
-		return errdefs.InvalidParameter(err)
+	if err := httputils.ReadJSON(r, execStartCheck); err != nil {
+		return err
 	}
 
 	if exists, err := s.backend.ExecExists(execName); !exists {
diff --git a/api/server/router/network/network_routes.go b/api/server/router/network/network_routes.go
index 69fc26a129..01114c8682 100644
--- a/api/server/router/network/network_routes.go
+++ b/api/server/router/network/network_routes.go
@@ -2,8 +2,6 @@ package network // import "github.com/docker/docker/api/server/router/network"
 
 import (
 	"context"
-	"encoding/json"
-	"io"
 	"net/http"
 	"strconv"
 	"strings"
@@ -205,23 +203,15 @@ func (n *networkRouter) getNetwork(ctx context.Context, w http.ResponseWriter, r
 }
 
 func (n *networkRouter) postNetworkCreate(ctx context.Context, w http.ResponseWriter, r *http.Request, vars map[string]string) error {
-	var create types.NetworkCreateRequest
-
 	if err := httputils.ParseForm(r); err != nil {
 		return err
 	}
 
-	if err := httputils.CheckForJSON(r); err != nil {
+	var create types.NetworkCreateRequest
+	if err := httputils.ReadJSON(r, &create); err != nil {
 		return err
 	}
 
-	if err := json.NewDecoder(r.Body).Decode(&create); err != nil {
-		if err == io.EOF {
-			return errdefs.InvalidParameter(errors.New("got EOF while reading request body"))
-		}
-		return errdefs.InvalidParameter(err)
-	}
-
 	if nws, err := n.cluster.GetNetworksByName(create.Name); err == nil && len(nws) > 0 {
 		return nameConflict(create.Name)
 	}
@@ -255,22 +245,15 @@ func (n *networkRouter) postNetworkCreate(ctx context.Context, w http.ResponseWr
 }
 
 func (n *networkRouter) postNetworkConnect(ctx context.Context, w http.ResponseWriter, r *http.Request, vars map[string]string) error {
-	var connect types.NetworkConnect
 	if err := httputils.ParseForm(r); err != nil {
 		return err
 	}
 
-	if err := httputils.CheckForJSON(r); err != nil {
+	var connect types.NetworkConnect
+	if err := httputils.ReadJSON(r, &connect); err != nil {
 		return err
 	}
 
-	if err := json.NewDecoder(r.Body).Decode(&connect); err != nil {
-		if err == io.EOF {
-			return errdefs.InvalidParameter(errors.New("got EOF while reading request body"))
-		}
-		return errdefs.InvalidParameter(err)
-	}
-
 	// Unlike other operations, we does not check ambiguity of the name/ID here.
 	// The reason is that, In case of attachable network in swarm scope, the actual local network
 	// may not be available at the time. At the same time, inside daemon `ConnectContainerToNetwork`
@@ -279,22 +262,15 @@ func (n *networkRouter) postNetworkConnect(ctx context.Context, w http.ResponseW
 }
 
 func (n *networkRouter) postNetworkDisconnect(ctx context.Context, w http.ResponseWriter, r *http.Request, vars map[string]string) error {
-	var disconnect types.NetworkDisconnect
 	if err := httputils.ParseForm(r); err != nil {
 		return err
 	}
 
-	if err := httputils.CheckForJSON(r); err != nil {
+	var disconnect types.NetworkDisconnect
+	if err := httputils.ReadJSON(r, &disconnect); err != nil {
 		return err
 	}
 
-	if err := json.NewDecoder(r.Body).Decode(&disconnect); err != nil {
-		if err == io.EOF {
-			return errdefs.InvalidParameter(errors.New("got EOF while reading request body"))
-		}
-		return errdefs.InvalidParameter(err)
-	}
-
 	return n.backend.DisconnectContainerFromNetwork(disconnect.Container, vars["id"], disconnect.Force)
 }
 
diff --git a/api/server/router/plugin/plugin_routes.go b/api/server/router/plugin/plugin_routes.go
index 8c36b51ecc..c82996679d 100644
--- a/api/server/router/plugin/plugin_routes.go
+++ b/api/server/router/plugin/plugin_routes.go
@@ -4,7 +4,6 @@ import (
 	"context"
 	"encoding/base64"
 	"encoding/json"
-	"io"
 	"net/http"
 	"strconv"
 	"strings"
@@ -13,7 +12,6 @@ import (
 	"github.com/docker/docker/api/server/httputils"
 	"github.com/docker/docker/api/types"
 	"github.com/docker/docker/api/types/filters"
-	"github.com/docker/docker/errdefs"
 	"github.com/docker/docker/pkg/ioutils"
 	"github.com/docker/docker/pkg/streamformatter"
 	"github.com/pkg/errors"
@@ -96,12 +94,8 @@ func (pr *pluginRouter) upgradePlugin(ctx context.Context, w http.ResponseWriter
 	}
 
 	var privileges types.PluginPrivileges
-	dec := json.NewDecoder(r.Body)
-	if err := dec.Decode(&privileges); err != nil {
-		return errors.Wrap(err, "failed to parse privileges")
-	}
-	if dec.More() {
-		return errors.New("invalid privileges")
+	if err := httputils.ReadJSON(r, &privileges); err != nil {
+		return err
 	}
 
 	metaHeaders, authConfig := parseHeaders(r.Header)
@@ -135,12 +129,8 @@ func (pr *pluginRouter) pullPlugin(ctx context.Context, w http.ResponseWriter, r
 	}
 
 	var privileges types.PluginPrivileges
-	dec := json.NewDecoder(r.Body)
-	if err := dec.Decode(&privileges); err != nil {
-		return errors.Wrap(err, "failed to parse privileges")
-	}
-	if dec.More() {
-		return errors.New("invalid privileges")
+	if err := httputils.ReadJSON(r, &privileges); err != nil {
+		return err
 	}
 
 	metaHeaders, authConfig := parseHeaders(r.Header)
@@ -277,11 +267,8 @@ func (pr *pluginRouter) pushPlugin(ctx context.Context, w http.ResponseWriter, r
 
 func (pr *pluginRouter) setPlugin(ctx context.Context, w http.ResponseWriter, r *http.Request, vars map[string]string) error {
 	var args []string
-	if err := json.NewDecoder(r.Body).Decode(&args); err != nil {
-		if err == io.EOF {
-			return errdefs.InvalidParameter(errors.New("got EOF while reading request body"))
-		}
-		return errdefs.InvalidParameter(err)
+	if err := httputils.ReadJSON(r, &args); err != nil {
+		return err
 	}
 	if err := pr.backend.Set(vars["name"], args); err != nil {
 		return err
diff --git a/api/server/router/swarm/cluster_routes.go b/api/server/router/swarm/cluster_routes.go
index 0751617450..05c10082a1 100644
--- a/api/server/router/swarm/cluster_routes.go
+++ b/api/server/router/swarm/cluster_routes.go
@@ -2,9 +2,7 @@ package swarm // import "github.com/docker/docker/api/server/router/swarm"
 
 import (
 	"context"
-	"encoding/json"
 	"fmt"
-	"io"
 	"net/http"
 	"strconv"
 
@@ -21,11 +19,8 @@ import (
 
 func (sr *swarmRouter) initCluster(ctx context.Context, w http.ResponseWriter, r *http.Request, vars map[string]string) error {
 	var req types.InitRequest
-	if err := json.NewDecoder(r.Body).Decode(&req); err != nil {
-		if err == io.EOF {
-			return errdefs.InvalidParameter(errors.New("got EOF while reading request body"))
-		}
-		return errdefs.InvalidParameter(err)
+	if err := httputils.ReadJSON(r, &req); err != nil {
+		return err
 	}
 	version := httputils.VersionFromContext(ctx)
 
@@ -48,11 +43,8 @@ func (sr *swarmRouter) initCluster(ctx context.Context, w http.ResponseWriter, r
 
 func (sr *swarmRouter) joinCluster(ctx context.Context, w http.ResponseWriter, r *http.Request, vars map[string]string) error {
 	var req types.JoinRequest
-	if err := json.NewDecoder(r.Body).Decode(&req); err != nil {
-		if err == io.EOF {
-			return errdefs.InvalidParameter(errors.New("got EOF while reading request body"))
-		}
-		return errdefs.InvalidParameter(err)
+	if err := httputils.ReadJSON(r, &req); err != nil {
+		return err
 	}
 	return sr.backend.Join(req)
 }
@@ -78,11 +70,8 @@ func (sr *swarmRouter) inspectCluster(ctx context.Context, w http.ResponseWriter
 
 func (sr *swarmRouter) updateCluster(ctx context.Context, w http.ResponseWriter, r *http.Request, vars map[string]string) error {
 	var swarm types.Spec
-	if err := json.NewDecoder(r.Body).Decode(&swarm); err != nil {
-		if err == io.EOF {
-			return errdefs.InvalidParameter(errors.New("got EOF while reading request body"))
-		}
-		return errdefs.InvalidParameter(err)
+	if err := httputils.ReadJSON(r, &swarm); err != nil {
+		return err
 	}
 
 	rawVersion := r.URL.Query().Get("version")
@@ -132,11 +121,8 @@ func (sr *swarmRouter) updateCluster(ctx context.Context, w http.ResponseWriter,
 
 func (sr *swarmRouter) unlockCluster(ctx context.Context, w http.ResponseWriter, r *http.Request, vars map[string]string) error {
 	var req types.UnlockRequest
-	if err := json.NewDecoder(r.Body).Decode(&req); err != nil {
-		if err == io.EOF {
-			return errdefs.InvalidParameter(errors.New("got EOF while reading request body"))
-		}
-		return errdefs.InvalidParameter(err)
+	if err := httputils.ReadJSON(r, &req); err != nil {
+		return err
 	}
 
 	if err := sr.backend.UnlockSwarm(req); err != nil {
@@ -216,11 +202,8 @@ func (sr *swarmRouter) getService(ctx context.Context, w http.ResponseWriter, r
 
 func (sr *swarmRouter) createService(ctx context.Context, w http.ResponseWriter, r *http.Request, vars map[string]string) error {
 	var service types.ServiceSpec
-	if err := json.NewDecoder(r.Body).Decode(&service); err != nil {
-		if err == io.EOF {
-			return errdefs.InvalidParameter(errors.New("got EOF while reading request body"))
-		}
-		return errdefs.InvalidParameter(err)
+	if err := httputils.ReadJSON(r, &service); err != nil {
+		return err
 	}
 
 	// Get returns "" if the header does not exist
@@ -243,11 +226,8 @@ func (sr *swarmRouter) createService(ctx context.Context, w http.ResponseWriter,
 
 func (sr *swarmRouter) updateService(ctx context.Context, w http.ResponseWriter, r *http.Request, vars map[string]string) error {
 	var service types.ServiceSpec
-	if err := json.NewDecoder(r.Body).Decode(&service); err != nil {
-		if err == io.EOF {
-			return errdefs.InvalidParameter(errors.New("got EOF while reading request body"))
-		}
-		return errdefs.InvalidParameter(err)
+	if err := httputils.ReadJSON(r, &service); err != nil {
+		return err
 	}
 
 	rawVersion := r.URL.Query().Get("version")
@@ -341,11 +321,8 @@ func (sr *swarmRouter) getNode(ctx context.Context, w http.ResponseWriter, r *ht
 
 func (sr *swarmRouter) updateNode(ctx context.Context, w http.ResponseWriter, r *http.Request, vars map[string]string) error {
 	var node types.NodeSpec
-	if err := json.NewDecoder(r.Body).Decode(&node); err != nil {
-		if err == io.EOF {
-			return errdefs.InvalidParameter(errors.New("got EOF while reading request body"))
-		}
-		return errdefs.InvalidParameter(err)
+	if err := httputils.ReadJSON(r, &node); err != nil {
+		return err
 	}
 
 	rawVersion := r.URL.Query().Get("version")
@@ -423,11 +400,8 @@ func (sr *swarmRouter) getSecrets(ctx context.Context, w http.ResponseWriter, r
 
 func (sr *swarmRouter) createSecret(ctx context.Context, w http.ResponseWriter, r *http.Request, vars map[string]string) error {
 	var secret types.SecretSpec
-	if err := json.NewDecoder(r.Body).Decode(&secret); err != nil {
-		if err == io.EOF {
-			return errdefs.InvalidParameter(errors.New("got EOF while reading request body"))
-		}
-		return errdefs.InvalidParameter(err)
+	if err := httputils.ReadJSON(r, &secret); err != nil {
+		return err
 	}
 	version := httputils.VersionFromContext(ctx)
 	if secret.Templating != nil && versions.LessThan(version, "1.37") {
@@ -464,11 +438,8 @@ func (sr *swarmRouter) getSecret(ctx context.Context, w http.ResponseWriter, r *
 
 func (sr *swarmRouter) updateSecret(ctx context.Context, w http.ResponseWriter, r *http.Request, vars map[string]string) error {
 	var secret types.SecretSpec
-	if err := json.NewDecoder(r.Body).Decode(&secret); err != nil {
-		if err == io.EOF {
-			return errdefs.InvalidParameter(errors.New("got EOF while reading request body"))
-		}
-		return errdefs.InvalidParameter(err)
+	if err := httputils.ReadJSON(r, &secret); err != nil {
+		return err
 	}
 
 	rawVersion := r.URL.Query().Get("version")
@@ -500,11 +471,8 @@ func (sr *swarmRouter) getConfigs(ctx context.Context, w http.ResponseWriter, r
 
 func (sr *swarmRouter) createConfig(ctx context.Context, w http.ResponseWriter, r *http.Request, vars map[string]string) error {
 	var config types.ConfigSpec
-	if err := json.NewDecoder(r.Body).Decode(&config); err != nil {
-		if err == io.EOF {
-			return errdefs.InvalidParameter(errors.New("got EOF while reading request body"))
-		}
-		return errdefs.InvalidParameter(err)
+	if err := httputils.ReadJSON(r, &config); err != nil {
+		return err
 	}
 
 	version := httputils.VersionFromContext(ctx)
@@ -542,11 +510,8 @@ func (sr *swarmRouter) getConfig(ctx context.Context, w http.ResponseWriter, r *
 
 func (sr *swarmRouter) updateConfig(ctx context.Context, w http.ResponseWriter, r *http.Request, vars map[string]string) error {
 	var config types.ConfigSpec
-	if err := json.NewDecoder(r.Body).Decode(&config); err != nil {
-		if err == io.EOF {
-			return errdefs.InvalidParameter(errors.New("got EOF while reading request body"))
-		}
-		return errdefs.InvalidParameter(err)
+	if err := httputils.ReadJSON(r, &config); err != nil {
+		return err
 	}
 
 	rawVersion := r.URL.Query().Get("version")
diff --git a/api/server/router/volume/volume_routes.go b/api/server/router/volume/volume_routes.go
index e08e724579..195bc8b409 100644
--- a/api/server/router/volume/volume_routes.go
+++ b/api/server/router/volume/volume_routes.go
@@ -2,14 +2,11 @@ package volume // import "github.com/docker/docker/api/server/router/volume"
 
 import (
 	"context"
-	"encoding/json"
-	"io"
 	"net/http"
 
 	"github.com/docker/docker/api/server/httputils"
 	"github.com/docker/docker/api/types/filters"
 	volumetypes "github.com/docker/docker/api/types/volume"
-	"github.com/docker/docker/errdefs"
 	"github.com/docker/docker/volume/service/opts"
 	"github.com/pkg/errors"
 )
@@ -47,16 +44,9 @@ func (v *volumeRouter) postVolumesCreate(ctx context.Context, w http.ResponseWri
 		return err
 	}
 
-	if err := httputils.CheckForJSON(r); err != nil {
-		return err
-	}
-
 	var req volumetypes.VolumeCreateBody
-	if err := json.NewDecoder(r.Body).Decode(&req); err != nil {
-		if err == io.EOF {
-			return errdefs.InvalidParameter(errors.New("got EOF while reading request body"))
-		}
-		return errdefs.InvalidParameter(err)
+	if err := httputils.ReadJSON(r, &req); err != nil {
+		return err
 	}
 
 	volume, err := v.backend.Create(ctx, req.Name, req.Driver, opts.WithCreateOptions(req.DriverOpts), opts.WithCreateLabels(req.Labels))
diff --git a/integration-cli/docker_api_exec_test.go b/integration-cli/docker_api_exec_test.go
index 3bf5d003f8..5d4dd2d2ab 100644
--- a/integration-cli/docker_api_exec_test.go
+++ b/integration-cli/docker_api_exec_test.go
@@ -18,6 +18,7 @@ import (
 	"github.com/docker/docker/integration-cli/checker"
 	"github.com/docker/docker/testutil/request"
 	"gotest.tools/v3/assert"
+	is "gotest.tools/v3/assert/cmp"
 	"gotest.tools/v3/poll"
 )
 
@@ -56,7 +57,7 @@ func (s *DockerSuite) TestExecAPICreateNoValidContentType(c *testing.T) {
 	}
 	b, err := request.ReadBody(body)
 	assert.NilError(c, err)
-	assert.Assert(c, strings.Contains(getErrorMessage(c, b), "Content-Type specified"), "Expected message when creating exec command with invalid Content-Type specified")
+	assert.Assert(c, is.Contains(getErrorMessage(c, b), "unsupported Content-Type header (test/plain): must be 'application/json'"))
 }
 
 func (s *DockerSuite) TestExecAPICreateContainerPaused(c *testing.T) {
diff --git a/integration/container/container_test.go b/integration/container/container_test.go
index 0402828a77..06dce0f776 100644
--- a/integration/container/container_test.go
+++ b/integration/container/container_test.go
@@ -2,6 +2,7 @@ package container // import "github.com/docker/docker/integration/container"
 
 import (
 	"net/http"
+	"runtime"
 	"testing"
 
 	"github.com/docker/docker/testutil/request"
@@ -9,34 +10,69 @@ import (
 	is "gotest.tools/v3/assert/cmp"
 )
 
+// TestContainerInvalidJSON tests that POST endpoints that expect a body return
+// the correct error when sending invalid JSON requests.
 func TestContainerInvalidJSON(t *testing.T) {
 	defer setupTest(t)()
 
+	// POST endpoints that accept / expect a JSON body;
 	endpoints := []string{
 		"/containers/foobar/exec",
+		"/containers/foobar/update",
 		"/exec/foobar/start",
 	}
 
+	// windows doesnt support API < v1.24
+	if runtime.GOOS != "windows" {
+		endpoints = append(
+			endpoints,
+			"/v1.23/containers/foobar/copy", // deprecated since 1.8 (API v1.20), errors out since 1.12 (API v1.24)
+		)
+	}
+
 	for _, ep := range endpoints {
 		ep := ep
-		t.Run(ep, func(t *testing.T) {
+		t.Run(ep[1:], func(t *testing.T) {
 			t.Parallel()
 
-			res, body, err := request.Post(ep, request.RawString("{invalid json"), request.JSON)
-			assert.NilError(t, err)
-			assert.Equal(t, res.StatusCode, http.StatusBadRequest)
+			t.Run("invalid content type", func(t *testing.T) {
+				res, body, err := request.Post(ep, request.RawString("{}"), request.ContentType("text/plain"))
+				assert.NilError(t, err)
+				assert.Check(t, is.Equal(res.StatusCode, http.StatusBadRequest))
 
-			buf, err := request.ReadBody(body)
-			assert.NilError(t, err)
-			assert.Check(t, is.Contains(string(buf), "invalid character 'i' looking for beginning of object key string"))
+				buf, err := request.ReadBody(body)
+				assert.NilError(t, err)
+				assert.Check(t, is.Contains(string(buf), "unsupported Content-Type header (text/plain): must be 'application/json'"))
+			})
 
-			res, body, err = request.Post(ep, request.JSON)
-			assert.NilError(t, err)
-			assert.Equal(t, res.StatusCode, http.StatusBadRequest)
+			t.Run("invalid JSON", func(t *testing.T) {
+				res, body, err := request.Post(ep, request.RawString("{invalid json"), request.JSON)
+				assert.NilError(t, err)
+				assert.Check(t, is.Equal(res.StatusCode, http.StatusBadRequest))
 
-			buf, err = request.ReadBody(body)
-			assert.NilError(t, err)
-			assert.Check(t, is.Contains(string(buf), "got EOF while reading request body"))
+				buf, err := request.ReadBody(body)
+				assert.NilError(t, err)
+				assert.Check(t, is.Contains(string(buf), "invalid JSON: invalid character 'i' looking for beginning of object key string"))
+			})
+
+			t.Run("extra content after JSON", func(t *testing.T) {
+				res, body, err := request.Post(ep, request.RawString(`{} trailing content`), request.JSON)
+				assert.NilError(t, err)
+				assert.Check(t, is.Equal(res.StatusCode, http.StatusBadRequest))
+
+				buf, err := request.ReadBody(body)
+				assert.NilError(t, err)
+				assert.Check(t, is.Contains(string(buf), "unexpected content after JSON"))
+			})
+
+			t.Run("empty body", func(t *testing.T) {
+				// empty body should not produce an 500 internal server error, or
+				// any 5XX error (this is assuming the request does not produce
+				// an internal server error for another reason, but it shouldn't)
+				res, _, err := request.Post(ep, request.RawString(``), request.JSON)
+				assert.NilError(t, err)
+				assert.Check(t, res.StatusCode < http.StatusInternalServerError)
+			})
 		})
 	}
 }
diff --git a/integration/network/network_test.go b/integration/network/network_test.go
index ec0546aa0e..00603094a2 100644
--- a/integration/network/network_test.go
+++ b/integration/network/network_test.go
@@ -62,9 +62,12 @@ func TestRunContainerWithBridgeNone(t *testing.T) {
 	assert.Check(t, is.Equal(stdout.String(), result.Combined()), "The network namespace of container should be the same with host when --net=host and bridge network is disabled")
 }
 
+// TestNetworkInvalidJSON tests that POST endpoints that expect a body return
+// the correct error when sending invalid JSON requests.
 func TestNetworkInvalidJSON(t *testing.T) {
 	defer setupTest(t)()
 
+	// POST endpoints that accept / expect a JSON body;
 	endpoints := []string{
 		"/networks/create",
 		"/networks/bridge/connect",
@@ -73,24 +76,47 @@ func TestNetworkInvalidJSON(t *testing.T) {
 
 	for _, ep := range endpoints {
 		ep := ep
-		t.Run(ep, func(t *testing.T) {
+		t.Run(ep[1:], func(t *testing.T) {
 			t.Parallel()
 
-			res, body, err := request.Post(ep, request.RawString("{invalid json"), request.JSON)
-			assert.NilError(t, err)
-			assert.Equal(t, res.StatusCode, http.StatusBadRequest)
+			t.Run("invalid content type", func(t *testing.T) {
+				res, body, err := request.Post(ep, request.RawString("{}"), request.ContentType("text/plain"))
+				assert.NilError(t, err)
+				assert.Check(t, is.Equal(res.StatusCode, http.StatusBadRequest))
 
-			buf, err := request.ReadBody(body)
-			assert.NilError(t, err)
-			assert.Check(t, is.Contains(string(buf), "invalid character 'i' looking for beginning of object key string"))
+				buf, err := request.ReadBody(body)
+				assert.NilError(t, err)
+				assert.Check(t, is.Contains(string(buf), "unsupported Content-Type header (text/plain): must be 'application/json'"))
+			})
 
-			res, body, err = request.Post(ep, request.JSON)
-			assert.NilError(t, err)
-			assert.Equal(t, res.StatusCode, http.StatusBadRequest)
+			t.Run("invalid JSON", func(t *testing.T) {
+				res, body, err := request.Post(ep, request.RawString("{invalid json"), request.JSON)
+				assert.NilError(t, err)
+				assert.Check(t, is.Equal(res.StatusCode, http.StatusBadRequest))
 
-			buf, err = request.ReadBody(body)
-			assert.NilError(t, err)
-			assert.Check(t, is.Contains(string(buf), "got EOF while reading request body"))
+				buf, err := request.ReadBody(body)
+				assert.NilError(t, err)
+				assert.Check(t, is.Contains(string(buf), "invalid JSON: invalid character 'i' looking for beginning of object key string"))
+			})
+
+			t.Run("extra content after JSON", func(t *testing.T) {
+				res, body, err := request.Post(ep, request.RawString(`{} trailing content`), request.JSON)
+				assert.NilError(t, err)
+				assert.Check(t, is.Equal(res.StatusCode, http.StatusBadRequest))
+
+				buf, err := request.ReadBody(body)
+				assert.NilError(t, err)
+				assert.Check(t, is.Contains(string(buf), "unexpected content after JSON"))
+			})
+
+			t.Run("empty body", func(t *testing.T) {
+				// empty body should not produce an 500 internal server error, or
+				// any 5XX error (this is assuming the request does not produce
+				// an internal server error for another reason, but it shouldn't)
+				res, _, err := request.Post(ep, request.RawString(``), request.JSON)
+				assert.NilError(t, err)
+				assert.Check(t, res.StatusCode < http.StatusInternalServerError)
+			})
 		})
 	}
 }
diff --git a/integration/plugin/common/plugin_test.go b/integration/plugin/common/plugin_test.go
index fb37a5e174..37ef0b3374 100644
--- a/integration/plugin/common/plugin_test.go
+++ b/integration/plugin/common/plugin_test.go
@@ -29,31 +29,61 @@ import (
 	"gotest.tools/v3/skip"
 )
 
+// TestPluginInvalidJSON tests that POST endpoints that expect a body return
+// the correct error when sending invalid JSON requests.
 func TestPluginInvalidJSON(t *testing.T) {
 	defer setupTest(t)()
 
-	endpoints := []string{"/plugins/foobar/set"}
+	// POST endpoints that accept / expect a JSON body;
+	endpoints := []string{
+		"/plugins/foobar/set",
+		"/plugins/foobar/upgrade",
+		"/plugins/pull",
+	}
 
 	for _, ep := range endpoints {
 		ep := ep
-		t.Run(ep, func(t *testing.T) {
+		t.Run(ep[1:], func(t *testing.T) {
 			t.Parallel()
 
-			res, body, err := request.Post(ep, request.RawString("{invalid json"), request.JSON)
-			assert.NilError(t, err)
-			assert.Equal(t, res.StatusCode, http.StatusBadRequest)
+			t.Run("invalid content type", func(t *testing.T) {
+				res, body, err := request.Post(ep, request.RawString("[]"), request.ContentType("text/plain"))
+				assert.NilError(t, err)
+				assert.Check(t, is.Equal(res.StatusCode, http.StatusBadRequest))
 
-			buf, err := request.ReadBody(body)
-			assert.NilError(t, err)
-			assert.Check(t, is.Contains(string(buf), "invalid character 'i' looking for beginning of object key string"))
+				buf, err := request.ReadBody(body)
+				assert.NilError(t, err)
+				assert.Check(t, is.Contains(string(buf), "unsupported Content-Type header (text/plain): must be 'application/json'"))
+			})
 
-			res, body, err = request.Post(ep, request.JSON)
-			assert.NilError(t, err)
-			assert.Equal(t, res.StatusCode, http.StatusBadRequest)
+			t.Run("invalid JSON", func(t *testing.T) {
+				res, body, err := request.Post(ep, request.RawString("{invalid json"), request.JSON)
+				assert.NilError(t, err)
+				assert.Check(t, is.Equal(res.StatusCode, http.StatusBadRequest))
 
-			buf, err = request.ReadBody(body)
-			assert.NilError(t, err)
-			assert.Check(t, is.Contains(string(buf), "got EOF while reading request body"))
+				buf, err := request.ReadBody(body)
+				assert.NilError(t, err)
+				assert.Check(t, is.Contains(string(buf), "invalid JSON: invalid character 'i' looking for beginning of object key string"))
+			})
+
+			t.Run("extra content after JSON", func(t *testing.T) {
+				res, body, err := request.Post(ep, request.RawString(`[] trailing content`), request.JSON)
+				assert.NilError(t, err)
+				assert.Check(t, is.Equal(res.StatusCode, http.StatusBadRequest))
+
+				buf, err := request.ReadBody(body)
+				assert.NilError(t, err)
+				assert.Check(t, is.Contains(string(buf), "unexpected content after JSON"))
+			})
+
+			t.Run("empty body", func(t *testing.T) {
+				// empty body should not produce an 500 internal server error, or
+				// any 5XX error (this is assuming the request does not produce
+				// an internal server error for another reason, but it shouldn't)
+				res, _, err := request.Post(ep, request.RawString(``), request.JSON)
+				assert.NilError(t, err)
+				assert.Check(t, res.StatusCode < http.StatusInternalServerError)
+			})
 		})
 	}
 }
diff --git a/integration/volume/volume_test.go b/integration/volume/volume_test.go
index f465e47b05..395c51e1f4 100644
--- a/integration/volume/volume_test.go
+++ b/integration/volume/volume_test.go
@@ -104,31 +104,57 @@ func TestVolumesInspect(t *testing.T) {
 	assert.Check(t, createdAt.Unix()-now.Unix() < 60, "CreatedAt (%s) exceeds creation time (%s) 60s", createdAt, now)
 }
 
+// TestVolumesInvalidJSON tests that POST endpoints that expect a body return
+// the correct error when sending invalid JSON requests.
 func TestVolumesInvalidJSON(t *testing.T) {
 	defer setupTest(t)()
 
+	// POST endpoints that accept / expect a JSON body;
 	endpoints := []string{"/volumes/create"}
 
 	for _, ep := range endpoints {
 		ep := ep
-		t.Run(ep, func(t *testing.T) {
+		t.Run(ep[1:], func(t *testing.T) {
 			t.Parallel()
 
-			res, body, err := request.Post(ep, request.RawString("{invalid json"), request.JSON)
-			assert.NilError(t, err)
-			assert.Equal(t, res.StatusCode, http.StatusBadRequest)
+			t.Run("invalid content type", func(t *testing.T) {
+				res, body, err := request.Post(ep, request.RawString("{}"), request.ContentType("text/plain"))
+				assert.NilError(t, err)
+				assert.Check(t, is.Equal(res.StatusCode, http.StatusBadRequest))
 
-			buf, err := request.ReadBody(body)
-			assert.NilError(t, err)
-			assert.Check(t, is.Contains(string(buf), "invalid character 'i' looking for beginning of object key string"))
+				buf, err := request.ReadBody(body)
+				assert.NilError(t, err)
+				assert.Check(t, is.Contains(string(buf), "unsupported Content-Type header (text/plain): must be 'application/json'"))
+			})
 
-			res, body, err = request.Post(ep, request.JSON)
-			assert.NilError(t, err)
-			assert.Equal(t, res.StatusCode, http.StatusBadRequest)
+			t.Run("invalid JSON", func(t *testing.T) {
+				res, body, err := request.Post(ep, request.RawString("{invalid json"), request.JSON)
+				assert.NilError(t, err)
+				assert.Check(t, is.Equal(res.StatusCode, http.StatusBadRequest))
 
-			buf, err = request.ReadBody(body)
-			assert.NilError(t, err)
-			assert.Check(t, is.Contains(string(buf), "got EOF while reading request body"))
+				buf, err := request.ReadBody(body)
+				assert.NilError(t, err)
+				assert.Check(t, is.Contains(string(buf), "invalid JSON: invalid character 'i' looking for beginning of object key string"))
+			})
+
+			t.Run("extra content after JSON", func(t *testing.T) {
+				res, body, err := request.Post(ep, request.RawString(`{} trailing content`), request.JSON)
+				assert.NilError(t, err)
+				assert.Check(t, is.Equal(res.StatusCode, http.StatusBadRequest))
+
+				buf, err := request.ReadBody(body)
+				assert.NilError(t, err)
+				assert.Check(t, is.Contains(string(buf), "unexpected content after JSON"))
+			})
+
+			t.Run("empty body", func(t *testing.T) {
+				// empty body should not produce an 500 internal server error, or
+				// any 5XX error (this is assuming the request does not produce
+				// an internal server error for another reason, but it shouldn't)
+				res, _, err := request.Post(ep, request.RawString(``), request.JSON)
+				assert.NilError(t, err)
+				assert.Check(t, res.StatusCode < http.StatusInternalServerError)
+			})
 		})
 	}
 }