The Chicago American Indian Center was created in 1953, at a time of great change for the Chicago Native community. Native peoples had been moving to and from Chicago since forced removal in the 1830s, but the Bureau of Indian Affairs's voluntary relocation program (1952-1972) meant that there was a significant increase in Chicago's Native population. In response to this change, a group of organizations including the Bureau of Indian Affairs (BIA), the Chicago Citizens’ Advisory Board, the American Indian Club, the Indian Council Fire, and the American Friends Service Committee began meeting in July of 1953 with the intention of creating connections between Native Americans moving to the city and the city itself. These meetings and the work of Native people already in the city led to the creation of the All-Tribes American Indian Center, which opened its doors in a rented space on LaSalle Drive in late 1953.

At the LaSalle location the American Indian Center began hosting annual powwows and formed clubs to facilitate community building in a growing intertribal Chicago Native community. The Canoe Club, the Photography Club, an all Native Boy Scout troop, a day camp, educational services, and job assistance were a few of the many clubs or programs developed in the first decade of the Center. Leaders within the American Indian Center and the Chicago Native community including Ben Bearskin, Frank Fastwolf, Tom Greenwood, Dorothy Holstein, Robinson Johnson, Willard LaMere, and many others participated in the planning for the famed Chicago American Indian Conference in July 1961 at the University of Chicago. The conference drew Native activists from across country to Chicago and resulted in drafting The Declaration of Indian Purpose, a document outlining the needs and priorities of Native communities that was delivered to President Kennedy.

In 1963, the center moved to North Broadway for several years, before moving to Uptown on West Wilson Avenue in 1967. Here the Center continued to host annual powwows, hold gatherings, develop programs, and participate in activism that asserted the presence of Native peoples in the city. In 2017, the American Indian Center moved out of Uptown and into its current location in Albany Park.

Over the past seventy years, the Center, its leadership, and the Chicago Native community have worked to uphold the legacy of the institution to serve the community and sustain the Center’s mission. It remains one of the oldest American Indian centers in the country.