[1] SR 400 begins at the south city limit of Alexandria at Hunting Creek.

The highway continues south into Fairfax County and Belle Haven as the George Washington Memorial Parkway toward Mount Vernon.

SR 400 is a four-lane divided highway through the Jones Point neighborhood before becoming undivided and crossing over the Capital Beltway (I-95 and I-495) on a freeway cap, a very wide overpass that shields the freeway from view of the crossing highway, between the Woodrow Wilson Bridge over the Potomac River and the Capital Beltway's interchange with U.S. Route 1 (US 1).

The first intersection north of the bridge is with Church Street, which receives a ramp from the westbound Capital Beltway.

SR 400 continues through Old Town Alexandria with six lanes and passes the Davis Chapel.