NY 364 was assigned as part of the 1930 renumbering of state highways in New York, but initially went no farther west than Middlesex.

The route heads west as Maple Avenue, passing north of the Penn Yan Central School District's campus before leaving the village for more rural areas of the town of Benton.

NY 364 crosses open farmland and rapidly ascends in elevation as it travels northwestward out of the valley surrounding Keuka Lake.

[3] After ascending 400 feet (122 m) in roughly 1.5 miles (2.4 km), the route begins to level off as it heads toward the town of Potter.

[4] In Potter, NY 364 turns to face due west, taking on a linear east–west alignment for most of its first 3 miles (5 km) in the town.

Past this point, NY 364 curves to the southwest,[3] descending roughly 300 feet (91 m) into another valley created by the West River as it approaches the hamlet of Middlesex on East Avenue.

North of the intersection, NY 364 turns to the northeast, running parallel to the lake as it crosses into Ontario County.

Over the next 1.5 miles (2.4 km), NY 364 and CR 11 slowly converge, with the two finally meeting at a junction just 700 feet (210 m) from the shore of Canandaigua Lake.

Here, the surroundings around NY 364 change substantially as the route serves a number of seaside homes and communities.

[3] The roadway continues north into the town of Canandaigua, with the surroundings initially remaining similar to those in Gorham.

[3] The portion of modern NY 364 southeast of North Vine Valley Road at Overacker Corners in Middlesex was state-maintained as early as 1926.