The Wheelwright Museum of the American Indian was founded in 1937 by Mary Cabot Wheelwright. Born into a wealthy Boston family, Wheelwright traveled widely and had a lifelong interest in the study of religions. Her collaborator in the establishment of the museum was Hastiin Klah, an esteemed and influential Navajo singer, or "medicine man." Klah was born in 1867, when most of Navajo people were held as prisoners of war by the United States government.
In the 1960s and 1970s the Navajo Nation exerted its independence through a number of sweeping changes, including the establishment of its own community college system. Also at that time Navajo singers founded the Navajo Medicine Men's Association. The teachings of traditional Navajo religion enjoyed a revival, and its practitioners began to express their concerns about the teaching of Navajo religion by anyone other than Navajos. In 1977 the museum's board of trustees acknowledged the wisdom and authority of the Navajo Medicine Man's Association by voting to repatriate several Navajo medicine bundles and other items to the Navajo people, who now maintain them at the Ned A. Hatathli Cultural Center Museum at Navajo Community College, Tsaile, Arizona.
With the repatriation of 1977, the museum changed its name to the Wheelwright Museum of the American Indian. Although it is no longer actively involved in the study of Navajo religion, it maintains growing, world-renowned collections that document Navajo art and culture from 1850 to the present. It also presents changing exhibitions on traditional and contemporary Navajo and other Native American arts.