Most of the alignment of NY 374 is located in the Adirondack Park, heading along the shorelines of several large lakes in the northern part of the park, including the two Chateaugay Lakes and Chazy Lake. The route serves as the major road in the area of the Adirondacks for most of its length, and as a major arterial in Plattsburgh. NY 374 was assigned in the 1930 state route renumbering from NY 3 in Cadyville to the state line. It was extended eastward to NY 22 in Plattsburgh in the 1970s following the completion of an arterial bypassing northern Plattsburgh. Until 2017, NY 374's western terminus was at the Canada–United States border north of the village of Chateaugay, where the road continued north as a local road to Route 202. This route is now maintained by Franklin County and designated as County Route 52.