During the Gold Rush, Moccasin was a stage coach stop on Big Oak Flat Road. A covered bridge spanned Moccasin Creek.

Today, Moccasin is a company town owned by the City and County of San Francisco.

The original Moccasin Powerhouse, which was built as a component of the Hetch Hetchy Project system, began generating electricity in 1925. The old powerhouse was replaced by a new powerhouse in 1969.