The bulkhead wharf and pier substructure were built in 1914. The bulkhead building and transit shed were built in 1915-1916. In 1919, the bulkhead building was connected to the Pier 33 bulkhead building when that structure was completed.

In 1933 the pier was lengthened by 78 feet and the walls were largely rebuilt.

For many years prior to 2014, Pier 35 was San Francisco's sole, spartan cruise terminal. On September 25, 2014, the newly-built James R. Herman Cruise Terminal began operations at Pier 27. Pier 35 still provides backup when more than one cruise ship is in port.

In 2020, the liberty ship Jeremiah O'Brien moved from Pier 45 to Pier 35 after a fire destroyed much of pier 45.

Pier 35 contributes to the Port of San Francisco Embarcadero Historic District which was listed on the National Register of Historic Places in 2006.