Founded in 1880 as the Indian University by missionary Almon C. Bacone, it was originally affiliated with the mission arm of what is now American Baptist Churches USA.

Renamed as Bacone College in the early 20th century, it is the oldest continuously operated institution of higher education in Oklahoma.

The liberal arts college has had strong historic ties to several tribal nations, including the Muscogee and Cherokee.

[4] According to historian John Bartlett Meserve, Bacone College can be traced to a Baptist mission school at Valley Town in western North Carolina, which was part of Cherokee homelands.

After most of the Cherokee were removed to Indian Territory in the late 1830s, the Valley Town school moved to a site near what developed as present-day Westville, Oklahoma.

Bacone appealed to the Muscogee Creek Nation's Tribal Council to donate 160 acres (0.65 km2) (a quarter section) of land for the college in nearby Muskogee.

It began to lay off most employees following commencement and reported that it needed an immediate infusion of $2 million in order to continue to operate: to complete the 2018–2019 academic year and to open in the fall of 2019.

[14][15] One day before the auction, it was called off; however, the school had already laid off the bulk of its teachers in anticipation and was trying to get its students enrolled in other colleges for the next semester.

"Old Rock," as it came to be called, served as classroom, dormitory, dining hall, chapel, teacher quarters and administration building.

A "stone bible" sculpture marks the spot on which President Bacone and Joseph Samuel Murrow and Daniel Rogers, two Baptist missionaries and trustees, knelt in prayer to dedicate the college.

This includes artwork by Richard "Dick" West (Southern Cheyenne), an alumnus, former director of the art department and professor emeritus.

The gallery also holds work by Woody Crumbo (Citizen Potawatomi), the only American Indian to receive a Julius Rosenwald Fellowship.

Collectively, the modernist Flatstyle painting movement developed by Blue Eagle, Crumbo, West, and others is known as the Bacone school.

[20] The college possesses the Ataloa Lodge Museum, built in 1932 and housing more than 20,000 pieces of traditional and contemporary Native American art, including the largest collection of Kachina dolls in the country.

[21][22] The fireplace of the lodge is constructed of stones sent to the college from various indigenous communities, and includes rocks from the grave of Sitting Bull, and from the field where Custer made his last stand.

[2] In January, 2022, the college officially opened the VanBuren Sunshine Gallery, being exhibition space in McCombs Hall used to display new student art.