The toll bridge was conceived as early as the California Gold Rush days, with "Emperor" Joshua Norton famously advocating for it, but construction did not begin until 1933. Designed by Charles H. Purcell, and built by the American Bridge Company, it opened on Thursday, November 12, 1936, six months before the Golden Gate Bridge. It originally carried automobile traffic on its upper deck, with trucks, cars, buses, and Commuter Trains on the lower, but after the key system abandoned rail service on April 20, 1958, the lower deck was converted to all-road traffic as well. On October 12, 1963, traffic was reconfigured to one-way traffic on each deck, westbound on the upper deck, and eastbound on the lower deck, with trucks and buses allowed on the upper deck.

In 1986, the bridge was unofficially dedicated to former California Governor James Rolph.

The bridge has two sections of roughly equal length; the older western section, officially known as the Willie L. Brown Jr. Bridge (after former San Francisco mayor and California State Assembly Speaker Willie E. Brown Jr.), connects downtown San Francisco to Yerba Buena Island, and the newer unnamed eastern section connects the island to Oakland. The western section is a double suspension bridge with two decks, with westbound traffic being carried on the upper deck while eastbound is carried on the lower one. The largest span of the original eastern section was a Cantilever Bridge. During the 1989 Loma Prieta Earthquake, a portion of the eastern section's upper deck collapsed onto the lower deck and the bridge was closed for a month. Reconstruction of the eastern section of the bridge as a causeway connected to a self-anchored suspension bridge began in 2002; the new eastern section opened September 2, 2013, at a reported cost of over $6.5 billion; the original estimate of $250 million was for a seismic retrofit of the existing span. Unlike the western section and the original eastern section of the bridge, the new eastern section is a single deck carrying all eastbound and westbound lanes. Demolition of the old east span was completed on September 8, 2018.