Instead, intersecting portions of the pre-existing towns of New Haven, Panton, and Ferrisburg at the Otter Creek Falls were combined to form Vergennes.

The city is named for Frenchman Charles Gravier, comte de Vergennes, who greatly aided the rebel colonial effort in the American Revolutionary War.

[9] Organizers chose a city form of municipal government in anticipation of developing the area as an industrial center.

The Otter Creek Falls provided power for mills and factories, and the close access to the Lake Champlain waterway was ideal for transportation both north and south.

Industry boomed in the late 19th century; in particular, shipping connected to the Champlain Canal and wood-finishing related to lumber imported from Canada.

In the early years of the 21st century, a group of civic boosters and merchants improved the downtown area along Main Street and reconnected the city to its waterways.

The resulting development, catering to tourists and transients, is hampered by centralization of land ownership and escalation of commercial rents.

[citation needed] In July 2022, Vergennes was reconnected to the national passenger rail network when Amtrak's Ethan Allen Express began serving Ferrisburgh–Vergennes station.

The city features the Vergennes Opera House, which has weekly events involving the community and special guests, bands, singers, politicians, and theater groups.

[citation needed] Vermont Route 22A runs through the city, and makes a junction with U.S. Highway 7 on the northern outskirts of Vergennes.