I-64 enters Virginia as a four-lane divided highway, continuing its concurrency with US 60 through Covington into Lexington where the two routes split.

Once on the south side of Downtown Richmond, I-64 diverges from its concurrency with I-95 and continues southeasterly down the Virginia Peninsula through New Kent County and the Historic Triangle, into Newport News.

[7] About a mile (1.6 km) before the southern interchange with State Route 199 (SR 199), I-64 becomes a six-lane divided highway as it continues toward Hampton Roads.

It then becomes a six-lane divided highway with a two-lane reversible roadway in the middle, which is used for HOV traffic during morning and afternoon rush hours.

It continues through Norfolk, curving multiple times and eventually ending up heading due south as it passes the interchange with another of its spur routes, I-264 on the northwest side of Virginia Beach.

I-64's lanes continue northbound as I-664 to Newport News across the Monitor–Merrimac Memorial Bridge–Tunnel (MMMBT), ending at I-64 in Hampton, completing the beltway.

[8][9][10][11] However, in the late 1950s, a number of interested citizens, including Virginia Senator Mosby Perrow Jr., proposed that I-64 be realigned to run along US 220, US 460, SR 307, and US 360 from Clifton Forge via Cloverdale (near Roanoke), Lynchburg, and Farmville to Richmond.

The decision was on hold for three years while the state continued planning for the piece of the US 250 alignment from Richmond to Short Pump, which would be needed anyway to handle traffic.

[12] In 1961, US Secretary of Commerce Luther H. Hodges rejected that plan and chose the present route, leaving Lynchburg as the largest city in Virginia not served by an Interstate.

Southside Similar to I-64 west of Newport News on the Peninsula, VDOT and the HRTPO undertook environmental and preliminary engineering studies for the improvement of the eight-mile (13 km), 48-year-old corridor of the I-64 from I-464 in Chesapeake to the Bower's Hill Interchange.

This included replacing the functionally obsolete High Rise Bridge, which was completed one year after the study corridor opened, in 1969.

[24] This is because most of the interchange ramps were built to previous Interstate standards and were based on then-rural development in the Western Chesapeake and Eastern Suffolk.

[25] In addition, since the start of tolling at the Elizabeth River Tunnels, the High Rise Bridge and the corridor has received a nearly seven-percent increase in traffic during peak hours, further exacerbating the problem.

Construction will be conducted in multiple phases, similar to the widening project on the Peninsula: Once completed, the entire corridor would be an eight-lane stretch of highway, with two 135-foot (41 m) fixed-span bridges.

[33] After nearly two decades of studies and planning, the CTB and the two regional boards responsible for the project (HRTPO/Hampton Roads Transportation Accountability Commission (HRTAC)) voted unanimously in 2016 to a $3.3-billion expansion of the current bridge–tunnel and its approaches from two to four lanes in both directions from the I-664 interchange to the I-564 interchange, with two new, two-lane bridge–tunnels built to carry traffic eastbound (Hampton to Norfolk).

A final environmental impact statement (EIS) was published in May 2017, and the Record of Decision (ROD) from the Federal Highway Administration (FHWA) was granted in June.