[1] It is named for the unincorporated community surrounding it, Bowers Hill, Virginia, which itself is a part of the independent city of Chesapeake.

The first portions of I-264 were opened beginning in 1964 and in 1966 were completed from Bowers Hill to the western approach to the Downtown Tunnel in Portsmouth.

The 22 miles (35 km) of I-64 between U.S. Route 460 (US 460) at Wards Corner in Norfolk and Bowers Hill in Chesapeake was completed in 1969.

One of the more recent portions of the Interstate Highway System to be built in Virginia, I-664, was completed in April 1992.

I-664 includes the 4.6-mile-long (7.4 km) Monitor-Merrimac Memorial Bridge-Tunnel across Hampton Roads between the independent cities of Newport News and Suffolk.

A similar bridge to the original overpass remains nearby on Military Highway, crossing the now-abandoned Virginian Railway bed.

Because of the way the I-64 terminates—it is heading westerly, but is technically I-64 East, VDOT dropped all directional signs west of I-264 in Virginia Beach.