The building was erected by the Louisiana Purchase Exposition Company. The agreement called for transfer of title to the City following the fair, in return for the use of the western half of Forest Park as part of the fairgrounds.

In 1907, the Museum became a municipal institution after approval by the city electorate of a tax levy for its support, making it the first art museum to be publicly maintained. It has since been developed into one of the foremost collections of fine arts in America. Since 1971 it has been under the control of the metropolitan Zoo-Museum Tax District, which also includes the Zoo, the Science Center, and the Missouri Botanical Garden.