The northern terminus of the route is at a junction with Lily Lake Road in the hamlet of Bleecker, where the highway continues north and west as County Route 112 (CR 112) to London Bridge Road (CR 111, near NY 10 and NY 29A) at West Caroga Lake in the town of Caroga.

At this point, the amount of development along NY 309 drops substantially as it parallels Cayadutta Creek and heads northwestward out of the city limits.

[4] 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.

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 highway continues its northeastward descent into the small lakeside hamlet of Bleecker, where NY 309 ends at an intersection with Lily Lake Road.