In the U.S. state of Vermont, U.S. Route 4 (US 4) extends for 66.06 miles (106.31 km) between the New York state line at Fair Haven and the New Hampshire state line at White River Junction. It is one of the main arteries between New York and New Hampshire.
Upon crossing into Vermont from New York, US 4 immediately expands from a two-lane highway to a four-lane expressway. US 4 changes from being signed north–south (in New York) to being signed east–west (in Vermont). The historic routing of US 4 runs nearby as VT 4A, which later becomes US 4 Business as it enters the town of Rutland.
The 19-mile (31 km) US 4 expressway was built in anticipation of the proposed, but never built, East-West Highway which was supposed to link the population centers of northern New England. As such, this section of freeway meets Interstate Highway standards. The freeway has junctions with VT 22A in Fair Haven and VT 30 in Castleton. In West Rutland, the last numbered exit on the highway, exit 6, leads to US 4 Business, which provides access to the town centers of West Rutland and Rutland town. The expressway veers south just outside the limits of Rutland city, ending at an at-grade intersection with US 7 south of the city.
US 4 overlaps with US 7 north into downtown Rutland, meeting the east end of its business route along the way. US 4 then leaves US 7 along Woodstock Avenue as it heads northeast out of the city. East of Rutland city, US 4 is a two-lane highway, meandering through the Green Mountains, passing by the town center of Mendon towards the town of Killington. In Killington, US 4 joins VT 100 as they pass through Killington center along the Ottauquechee River valley until the village of West Bridgewater at the Bridgewater town line. VT 100 splits off to the south while US 4 continues following the Ottauquechee River east through Bridgewater center into the town of Woodstock. Several miles later, US 4 enters the incorporated village of Woodstock, where it meets VT 12 and VT 106. Southbound VT 12 and eastbound US 4 overlap for about 4 miles (6.4 km) along the river and split at the village of Taftsville, in the northwest corner of the town of Hartland.
US 4 continues following the Ottauquechee River into the town of Hartford, passing through Quechee State Park and circling south of Deweys Pond to cross the river on the Quechee Gorge Bridge, before heading north to the south bank of the White River. Here, US 4 has an interchange with Interstate 89, then turns eastward following the river bank into the village of White River Junction. In the village, US 4 joins US 5 as they cross the White River. At a four-way intersection immediately after the crossing, US 5 continues north, VT 14 begins to the west, and US 4 continues to the east. US 4 crosses the New Hampshire state line at the Connecticut River after a quarter of a mile.