[3] Upon crossing into Vermont from New York, US 4 immediately expands from a two-lane highway to a four-lane expressway.

East of Rutland, US 4 is a two-lane highway, meandering through the Green Mountains and passing by the towns of Mendon and Killington.

VT 100 splits off to the south while US 4 continues following the Ottauquechee River east through Bridgewater center into the town of Woodstock.

Southbound VT 12 and eastbound US 4 overlap for about four miles (6.4 km) along the river and split in the Taftsville Historic District, in the northwest corner of the town of Hartland.

US 4 crosses the New Hampshire state line at the Connecticut River on the Lyman Bridge after a quarter of a mile (0.40 km).

Two years later, the western segment from the New York line in Fair Haven to exit 5 also opened.

The construction of the eastern segment (from exit 6 to the intersection with US 7) was delayed for several years and did not open to traffic until 1986.