[3] The route starts paralleling Butternut Creek through town, entering the hamlet of Copes Corners, where NY 51 junctions with CR 3.

NY 51 winds north along Butternut Creek, soon gaining the moniker of Marion Avenue as it reaches the village of Gilbertsville.

The route soon junctions with Reservoir Road, which marks the northern end of Gilbertsville and access to Butternuts Cemetery.

[3] NY 51 continues through Morris, reaching a junction with the southern terminus of CR 49 in the rural hamlet of Elm Grove.

Passing north of a mobile home park, the route begins to bend northward and enters the town of New Lisbon, where it junctions with the western terminus of CR 12, which connects to the namesake hamlet.

[3] After a curve near High Street, NY 51 leaves Garrattsville, reaching the eastern terminus of CR 17, soon crossing into the town of Burlington.

Continuing north through Burlington, NY 51 reaches the hamlet of Chapinville, where it turns eastward for a short distance at Arnold Road.

Crossing a small creek, the route soon turns northward at Gardner Road, reaching the hamlet of Burlington Flats.

[3] At Burlington Flats, NY 51 turns northeast at Washburn Road, crossing two junctions with CR 19.

After CR 19, the route retains its rural nature through Burlington, soon reaching the hamlet of West Exeter.

After a gradual curve, the route soon turns northwest and crosses the Herkimer County line just north of a junction with CR 21.

[3] Now in the town of Winfield, NY 51 crosses a junction with Truax and Forks Road (unsigned CR 162).

NY 51 and US 20 become concurrent along East Main Street, crossing north of Winfield Memorial Town Park, soon leaving the village.

Crossing a former railroad line, the route bypasses Cedarville Station, which is connected via a junction with Chepachet Road (CR 75).

2 and crosses into the town of German Flatts, soon reaching the hamlet of South Ilion, where it meets a junction with CR 51.