NY 374 was assigned as part of the 1930 renumbering of state highways in New York. It initially began at the Canada–United States border north of the village of Chateaugay and ended at an intersection with NY 3 in Cadyville, a small hamlet within the town of Plattsburgh. At the time, NY 3 was the primary east–west highway into the city of Plattsburgh. In the early 1970s, a new highway was constructed north of NY 3 between NY 374 and NY 22 just outside the Plattsburgh city limits. The roadway effectively supplanted NY 3 as the main east–west road into the city; in fact, a section of the highway was built within of NY 3. The highway was completed by 1973 as an eastward extension of NY 374.