It continues on the east side of the Southern Branch Elizabeth River in the South Norfolk neighborhood of Chesapeake.

[2] The name remains after it enters Portsmouth via the Hodges Ferry Bridge, including a short concurrency with US 460 Alt.

[3] At the Jordan Bridge, SR 337 again enters Chesapeake, heading east on Poindexter Street across I-464 and north on Bainbridge Boulevard.

The 1.09 miles (1.75 km) downtown Norfolk route uses Waterside Drive and Boush Street between the Berkley Bridge (SR 337/I-264/US 460 Alt.)

The route runs by major attractions such as Waterside Marketplace, Town Point Park, and Nauticus.

[4][5] By 1939,[6] SR 337 existed along 21st Street and Hampton Boulevard from Granby Street (part of State Route 27, State Route 170 after 1940[7]) near downtown Norfolk north to the Newport News Ferry at Sewell's Point.

[8][9] It was initially part of US 17, but in the early 1930s US 17 was rerouted west of Norfolk via the James River Bridge, bypassing both ferries.

However, at the same time, a new alternate route was created, entirely concurrent with US 460 (Poindexter Street, Wilson Road, Campostella Road, and Brambleton Avenue) between Bainbridge Boulevard in South Norfolk and Bank Street in downtown Norfolk.

[16] When the Berkley Bridge replacement was being planned, it was temporarily assigned the State Route 337 Alternate designation in 1951, pending the completion of the "Norfolk Traffic Study".

On the downtown side it exited onto City Hall Avenue, rejoining the former SR 337 at Bank Street.

Part of the former SR 337 was deleted, but US 58 continued to use Main Street between Commercial Place (the Portsmouth Ferry approach) and the north end of the old Berkley Bridge[18] until the Downtown Tunnel opened.

Coming off the bridge into downtown Norfolk, SR 337 instead turned east at City Hall Avenue, running onto Tidewater Drive along with US 58.

It turned off Tidewater Drive at Brambleton (there US 460), running west and northwest to the new Midtown Tunnel interchange.

A direct connection was also built at that time from the Jordan Bridge to the intersection of Bainbridge Boulevard and Poindexter Street, in conjunction with a full interchange at I-464.

The section on Park Avenue was removed, along with the concurrency with US 460 and SR 166, in favor of the direct connection.