The highway initially heads to the northeast as a four-lane, city-maintained road,[4] following Northern Boulevard along the south side of Wolfert's Roost Country Club and the northern edge of a housing tract.

After a quarter-mile (0.4 km), the route turns northward onto Van Rensselaer Boulevard, another four-lane street divided by a narrow median.

The route runs past two blocks of homes before leaving the Albany city limits[5] and becoming state-maintained as it crosses into the town of Colonie and its village of Menands.

The northern terminus of NY 377 also serves as the south entrance to Albany Rural Cemetery.

[2][3] The alignment of NY 377 has not changed since that time; however, the junction at the south end of the route was reconfigured into an interchange when the portion of US 9 in northern Albany was converted into a limited-access highway in the 1970s.