Now in the town of Johnstown, the route winds its way northwestward as it follows Cayadutta Creek through an area of hilly terrain south of Adirondack Park. Development along the route largely ends at the intersection with West State Street; however, a pair of isolated homes are situated on NY 309 about to the northeast ahead of an intersection with CR 122, an east–west highway that serves the Fulton County Infirmary a short distance to the west. The route continues to wind its way through the mountains to the hamlet of West Bush, where Cayadutta Creek ends amidst a small cluster of houses. The route turns north at this point, passing a handful of homes before leaving the community upon passing through a narrow pass between two hills.