diff --git a/jupyter_server/services/contents/handlers.py b/jupyter_server/services/contents/handlers.py
index 83db1f99ee..bdd0afbbd0 100644
--- a/jupyter_server/services/contents/handlers.py
+++ b/jupyter_server/services/contents/handlers.py
@@ -194,10 +194,6 @@ async def post(self, path=""):
         if file_exists:
             raise web.HTTPError(400, "Cannot POST to files, use PUT instead.")
 
-        dir_exists = await ensure_async(cm.dir_exists(path))
-        if not dir_exists:
-            raise web.HTTPError(404, "No such directory: %s" % path)
-
         model = self.get_json_body()
 
         if model is not None:
diff --git a/jupyter_server/services/contents/manager.py b/jupyter_server/services/contents/manager.py
index 2a2cf0c4b7..654fdba4e5 100644
--- a/jupyter_server/services/contents/manager.py
+++ b/jupyter_server/services/contents/manager.py
@@ -586,6 +586,7 @@ def copy(self, from_path, to_path=None):
         from_path must be a full path to a file.
         """
         path = from_path.strip("/")
+
         if to_path is not None:
             to_path = to_path.strip("/")
 
@@ -601,12 +602,20 @@ def copy(self, from_path, to_path=None):
         if model["type"] == "directory":
             raise HTTPError(400, "Can't copy directories")
 
-        if to_path is None:
+        is_destination_specified = to_path is not None
+        if not is_destination_specified:
             to_path = from_dir
         if self.dir_exists(to_path):
             name = copy_pat.sub(".", from_name)
             to_name = self.increment_filename(name, to_path, insert="-Copy")
             to_path = "{0}/{1}".format(to_path, to_name)
+        elif is_destination_specified:
+            if "/" in to_path:
+                to_dir, to_name = to_path.rsplit("/", 1)
+                if not self.dir_exists(to_dir):
+                    raise HTTPError(404, "No such parent directory: %s to copy file in" % to_dir)
+        else:
+            raise HTTPError(404, "No such directory: %s" % to_path)
 
         model = self.save(model, to_path)
         return model
@@ -946,6 +955,7 @@ async def copy(self, from_path, to_path=None):
         from_path must be a full path to a file.
         """
         path = from_path.strip("/")
+
         if to_path is not None:
             to_path = to_path.strip("/")
 
@@ -960,12 +970,21 @@ async def copy(self, from_path, to_path=None):
         model.pop("name", None)
         if model["type"] == "directory":
             raise HTTPError(400, "Can't copy directories")
-        if to_path is None:
+
+        is_destination_specified = to_path is not None
+        if not is_destination_specified:
             to_path = from_dir
         if await ensure_async(self.dir_exists(to_path)):
             name = copy_pat.sub(".", from_name)
             to_name = await self.increment_filename(name, to_path, insert="-Copy")
             to_path = "{0}/{1}".format(to_path, to_name)
+        elif is_destination_specified:
+            if "/" in to_path:
+                to_dir, to_name = to_path.rsplit("/", 1)
+                if not await ensure_async(self.dir_exists(to_dir)):
+                    raise HTTPError(404, "No such parent directory: %s to copy file in" % to_dir)
+        else:
+            raise HTTPError(404, "No such directory: %s" % to_path)
 
         model = await self.save(model, to_path)
         return model
diff --git a/tests/services/contents/test_manager.py b/tests/services/contents/test_manager.py
index 04608dc6e1..b8b6fd5ca6 100644
--- a/tests/services/contents/test_manager.py
+++ b/tests/services/contents/test_manager.py
@@ -657,11 +657,20 @@ async def test_copy(jp_contents_manager):
     copy2 = await ensure_async(cm.copy(path, "å b/copy 2.ipynb"))
     assert copy2["name"] == "copy 2.ipynb"
     assert copy2["path"] == "å b/copy 2.ipynb"
+
     # copy with specified path
     copy2 = await ensure_async(cm.copy(path, "/"))
     assert copy2["name"] == name
     assert copy2["path"] == name
 
+    # copy to destination whose parent dir does not exist
+    with pytest.raises(HTTPError) as e:
+        await ensure_async(cm.copy(path, "å x/copy 2.ipynb"))
+
+    copy3 = await ensure_async(cm.copy(path, "/copy 3.ipynb"))
+    assert copy3["name"] == "copy 3.ipynb"
+    assert copy3["path"] == "copy 3.ipynb"
+
 
 async def test_mark_trusted_cells(jp_contents_manager):
     cm = jp_contents_manager