In 1864 Don Juan Forster built the bunkhouse with adobe walls, dirt floors, and tile roof. It was used to house the vaqueros or cowboys who worked on the Rancho Santa Margarita. There were other bunkhouses scattered around the outlying areas, but this was the main bunkhouse.
It was made into a museum in 1965 during the command of Major General Robert E. Cushman, Jr. It was later expanded in 1971 and again in 1978. Present at the 1978 rededication ceremony was James Roosevelt, a former Marine LtCol, and son of President Franklin D. Roosevelt.
The bell located near the entrance to the Bunkhouse was donated to the Ranch House in 1988. It is a replica of the bells placed along the original route of El Camino Real in 1906. They commemorate the mission bells seen in each of the 21 missions along the King's Highway. The pipe from which they hang is shaped to represent a shepherd's crook.
Currently, the museum consists of five rooms: the Tack Room, the Bunkroom, the Tomaino Room, Jerome O’Neill’s Bedroom and the Museum Gallery.