The Oak Street Bridge opened in June 1957. During the planning, it was the "New Marpole Bridge" and steel plate girders salvaged from the second Granville Street Bridge made barges for constructing the foundations of the Oak Street Bridge.
After the bridge opened, traffic began to move several blocks to the east. The business districts along Hudson Street and Marine Drive went into a swift decline.
Tolls were charged for two years and $1 million was collected in the last year. Tolls were removed from all of the bridges in the Lower Mainland in the 1960s, although the recently opened Golden Ears and Port Mann bridges utilize electronic tolling systems.
The Oak Street Bridge was meant to partially replace the Marpole Bridge, just to the west, connecting Vancouver to Sea Island, on which the Vancouver International Airport is located. The Marpole Bridge was dismantled the same year the Oak Street Bridge opened.