In the U.S. state of Virginia, US 1 runs north–south through South Hill, Petersburg, Richmond, Fredericksburg, and Alexandria on its way from North Carolina to the 14th Street bridges into the District of Columbia.

It is completely paralleled by Interstate Highways in Virginia—Interstate 85 (I-85) south of Petersburg, I-95 north to Alexandria, and I-395 into the District of Columbia—and now serves mainly local traffic.

The U.S. Route heads north as a two-lane road, passes to the east of Palmer Springs, and crosses Lake Gaston, an impoundment of the Roanoke River.

The mainline highway and business route enter the town of South Hill along Danville Street, a two-lane road with center turn lane.

The U.S. Route meets the southern end of SR 138 (Union Mill Road), then expands to a four-lane divided highway for its four-ramp partial cloverleaf interchange with I-85 before leaving the town of South Hill.

The highway has a diamond interchange with I-85, then passes through the southern edge of the town of Alberta, where the U.S. Route meets the eastern end of SR 136 (Church Street).

US 1 reduces to three lanes a short distance north of the river and passes through the town of McKenney, where the highway intersects SR 40 (Doyle Boulevard).

Northeast of Dinwiddie, US 1 passes under I-85 with no access and meets the eastern end of Airport Street, which comprises the westernmost segment of US 460 Bus.

The routes expand to a four-lane divided highway at its intersection with SR 142 (Simpson Road), then they meet I-85 and US 460 at a six-ramp partial cloverleaf interchange.

After passing under CSX Transportation's North End Subdivision rail line, the highways split into a one-way pair, with northbound US 1 and eastbound US 460 Bus.

US 1 continues into Petersburg Old Town Historic District, where the highway intersects Bank and Bolingbrook streets, which is the northern terminus of US 301 Alt.

The highways pass along the western edge of residential Chesterfield Highlands Historic District before intersecting SR 144 (Temple Avenue), which joins the U.S.

The three highways pass under CSX Transportation's North End Subdivision, then cross Swift Creek into Chesterfield County, where SR 144 splits northwest onto Harrowgate Road at Pickadat Corner.

US 1 and US 301 continue along four-lane Jefferson Davis Highway, which passes under the CSX Transportation rail line and intersects SR 10 (West Hundred Road) on the eastern edge of Chester.

The highways intersect US 60 (Semmes Avenue), then veer north onto the Robert E. Lee Memorial Bridge, which the bifurcated James River and Belle Isle.

The highways intersect Byrd and Cumberland streets, a one-way pair that provide access to SR 195 (Downtown Expressway) in between.

North of the Little River, the route passes through Doswell, where it meets the western end of SR 30 (Kings Dominion Boulevard).

The highway meets SR 3 (William Street) at a cloverleaf interchange, passes under a pedestrian bridge along the edge of the University of Mary Washington, and crosses over the Rappahannock Canal.

US 1 has a grade-separated junction with SR 8900 (Centreport Parkway), which serves Stafford Regional Airport, before crossing Potomac Creek.

North of Aquia, US 1 enters the property of Marine Corps Base Quantico, within which the highway crosses Chopawamsic Creek into Prince William County.

Immediately north of the county line, the route has a partial cloverleaf interchange with Russell Road, a major highway within the military base.

US 1 passes the National Museum of the Marine Corps before its intersection at Triangle with SR 619 (Fuller Road), which leads east to the town of Quantico.

At SR 619, US 1 leaves the base property and briefly expands to a six-lane divided highway, then splits onto separate carriageways—Fraley Boulevard northbound and Main Street southbound—to pass through the town of Dumfries, within which the U.S. Route crosses Quantico Creek.

The U.S. Route meets the eastern end of SR 294 (Prince William Parkway) and begins to parallel the RF&P Subdivision rail line.

US 1 passes Woodbridge station, which is served by Amtrak and Virginia Railway Express, shortly before its junction with SR 123 (Gordon Boulevard).

Within the military property, US 1 crosses Accotink Creek, meets the southern end of SR 286 (Fairfax County Parkway), and passes under an overpass of a road within the base.

US 1 veers northeast and expands to eight lanes at Huntington Avenue and maintains that width until its major interchange with the Capital Beltway (I-95 and I-495) at Cameron Run on the boundary between Fairfax County and the independent city of Alexandria.

Metroway merges with the main streams of US 1 traffic, which expand to three lanes each way as the highway approaches the northern city limit at Four Mile Run.

US 1—again bearing the name Richmond Highway—continues through the urban village of Crystal City, where the highway has a trumpet interchange with SR 233, a connector to Ronald Reagan Washington National Airport.

[11] In 1975, the interchange between I-395 and US 1 was rebuilt, and originally there were plans to upgrade US 1 to Interstate 595 (I-595) southward to the connector road with Ronald Reagan Washington National Airport.