VT 17 was initially much shorter than it is today, extending from the Champlain Bridge to Addison upon assignment.

West of Bristol, the route passes through generally level terrain and connects multiple communities.

As the route approaches the village of Bristol, it meets VT 116 at an intersection just west of the community.

The route crosses into Chittenden County, as well as the Camel's Hump State Park, shortly afterward.

[4] The road connecting the ferry landing at Chimney Point to the town center of Addison was designated as VT F-7 ca.

The rest of the McCullough Turnpike to VT 100 in Waitsfield became part of the state highway system in 1956.

[7] The VT 17 designation was extended eastward through Chittenden County and along the McCullough State Highway at this time.

[10][11] VT 17's connection to the state of New York was temporarily severed in October 2009 when the Champlain Bridge was closed due to safety concerns.