The adaptive reuse of the building to a museum was funded as a Public Works Administration (WPA) project and carried out by the CCC. At the time of its opening in 1938, it was the only museum in the world owned by an American Indian tribe. After a year of expansion and remodeling funded by the Bureau of Indian Affairs, the museum was reopened on September 30, 1967. Once again, in 1994, the museum reopened after several months of additional renovations.
On October 15, 1987 the Osage Tribal Museum was placed on the National Register of Historic Places and on May 2, 2008 the museum celebrated its 70th anniversary.

The museum’s collection of over 6,000 objects began with the Tribal Council’s purchase of the John L. Bird collection in 1923.