The office of Superintendent of Public Instruction was created by the 1872 Montana Territorial Legislative Assembly to replace the older office of school commissioner. The Montana Constitution of 1889 made the office elective and defined its functions. In 1959 the Montana Legislative Assembly created the Department of Public Instruction to administer the office under the direction of the Superintendent of Public Instruction.

The United States Congress passed the Johnson-O'Malley Act in 1934 to provide funding for public school districts on Indian reservations. The payments were in lieu of taxes to compensate for the tax exempt reservation lands. Until 1946 financial arrangements were made between the local Indian agency office and the local school board. In 1946 the Division of Indian Education was established within the Office of Superintendent of Public Instruction to negotiate contracts directly with the U.S. Bureau of Indian Affairs. Gradually BIA schools were abandoned in favor of local school board-controlled schools. Starting in 1964 Public Law 874 regulated most of the funding of reservation schools, and Johnson-O'Malley funds were used primarily to fund special projects. Among the supervisors of Indian Education were Knute W. Bergen, William C. Howard, Earl J. Barlow, Dorrance D. Steele, and Robert W. Parsley. In addition superintendents Mary M. Condon, Harriet E. Miller, and Dolores Colburg handled much of the division's affairs directly. From 1975 to 1977 Bill Yellowtail served as assistant supervisor.