VT 35 begins at the intersection with VT 30 in Townshend. It runs northeast, intersecting with VT 121 in the Cambridgeport section of Grafton, approximately west of the border with New Hampshire. VT 35 and VT 121 run concurrently to the northwest for a few miles into the center of Grafton. VT 121 splits off to the west, while VT 35 turns due north, continuing into the town of Chester, where it ends at an intersection with VT 11. A short section of VT 35 in Athens was gravel until 2018, when the road was fullypaved.