After roughly 0.5 miles (0.8 km), it crosses over the Genesee River and into the town of Rush, becoming Rush–Scottsville Road in the process.

Past NY 15, the route reverts to a two-lane highway and veers southeast to parallel Honeoye Creek into the hamlet of Rush.

Here, the route passes through a more populated area as it intersects NY 15A in the center of the community, at which point it becomes Rush–Mendon Road.

About 0.5 miles (0.8 km) from NY 64, the open surroundings return as the route crosses into the Ontario County town of Victor.

NY 251 continues on a virtual east–west line for its first 1.5 miles (2.4 km) in the county, heading through slightly more developed but still sparsely populated areas.

At Phillips Road, the route curves southeastward for 1 mile (1.6 km) before making one final turn to the northeast.

[7] When the first set of posted routes were assigned in New York in 1924, this piece of modern NY 251 did not receive a designation.

The southwestern end of NY 35 was moved to Mumford c. 1938, shifting the location of the overlap to Main Street in Scottsville.