NY 314 extends for 0.76 miles (1.22 km) through the Clinton County town of Plattsburgh from Interstate 87 (I-87) exit 39 to U.S. Route 9.

The route heads northwestward as Ferry Road, passing by a small number of homes situated amongst open fields.

The route turns north onto West Shore Road, following the roadway along Lake Champlain and into the town of Grand Isle.

While on Allen Road, the route passes through an area of open fields and forests that contains only a couple dozen homes.

The primary highway leading from the New York ferry landing to US 9 near Plattsburgh, then Cumberland Head Road, was initially unnumbered.

[6][7] VT F-3 was maintained by the towns of South Hero and Grand Isle until June 20, 1957, when the state of Vermont assumed ownership and maintenance of the highway.

[5] The idea of a building a new highway that would lead directly from US 9 to the ferry landing at the southern tip of Cumberland Head was first proposed in 1964.

[14] The proposal finally gained traction in 2002 when New York State Senator Ronald B. Stafford was able to procure most of the $7.3 million required to build the highway.

[15] The Cumberland Head connector began at the east end of the divided highway portion of NY 314 and would pass through the rural interior of the peninsula on its way to the ferry landing.

[18] Following the completion of the project, ownership and maintenance of Cumberland Head Road (NY 314's former routing) was to be transferred from Clinton County to the town of Plattsburgh.

Some residents criticized the layout, stating that it made it difficult to travel to and from MacDonough Highway and Cumberland Head Road.