The portion of NY 351 north of the hamlet of Poestenkill was originally designated as New York State Route 153 in the 1930s.

This designation was removed in the 1940s, and the West Sand Lake–Cropseyville roadway became County Route 77 (CR 77) sometime afterward.

[3] After 2 miles (3.2 km) of little to no development, NY 351 enters the hamlet of Poestenkill, the northernmost community of significance along the route.

[2][5] The route continues north from Poestenkill as White Church Road, winding its way through the open and hilly terrain of the northern part of the town.

The terrain's complexion remains the same in the adjacent town of Brunswick, where the highway changes names to Farm to Market Road.