It runs from a junction with I-64 and I-664 (Hampton Roads Beltway) near Bower's Hill in Chesapeake east into Portsmouth and through the Downtown Tunnel under the Southern Branch Elizabeth River into Norfolk.

This interchange, which also serves the Norfolk Naval Shipyard, is where the Interstate reduces to four lanes and descends into the Downtown Tunnel under the Southern Branch Elizabeth River.

I-264 curves north as an eight-lane highway that crosses the Eastern Branch Elizabeth River on a drawbridge.

[6] I-264 continues east as an eight-lane freeway between the Eastern Branch Elizabeth River to the south and Hampton Roads Transit's Tide Light Rail tracks to the north.

East of US 460, the freeway passes to the south of Norfolk State University and has a diamond interchange with SR 405 (Ballentine Boulevard).

The first two interchanges in Virginia Beach, a partial cloverleaf junction with SR 190 (Witchduck Road) and a cloverleaf interchange with SR 225 (Independence Boulevard), serve the Pembroke Manor area, which is the central business district of the city.

Independence Boulevard also leads southeast toward Mount Trashmore Park, a reused landfill that is visible from the freeway, and further on toward the Virginia Beach Amphitheater and eventually the city's government center at Princess Anne.

The Interstate crosses Great Neck Creek and has its final interchange, a partial interchange with Bird Neck Road that provides an alternative route to the oceanfront, before approaching its eastern terminus at Parks Avenue just north of the Virginia Beach Convention Center.

The expressway ran from an interchange with I-64 and I-264 in Norfolk almost due east to the oceanfront area of Virginia Beach.

Technical errors were common; alarms installed to alert police of a nonpaying motorist would often be activated by the machine's failure to detect the insertion of the proper toll.

This is now the point where I-264 intersects and crosses the I-64 portion of the Hampton Roads Beltway near Military Circle Mall in Norfolk.