The Creek Council House was constructed in 1878 by the Muscogee Nation (Creek Nation) for use as their tribal capitol. This was the second incarnation of the Creek Council House. The first was established a few years earlier, but it was built of wood and in turn was very flimsy. The Muscogee people decided to build a more permanent structure in what is now known as Okmulgee.
In 1906, Creek Indian Sovereignty was abolished by the United States Government. All government offices ran by the Creek Indian then went into the possession of the Department of the Interior. The City of Okmulgee then purchased the site in 1919.
Establishment of the Creek Council House Museum in Okmulgee came in 1923 when many residents decided to preserve the Creek heritage for future generations.
Currently, there is a debate about whether to sell the property back to the Creek Indian. While the ownership of the property may change hands, its function as a museum will remain the same, no matter what is decided.
Even though the old Muscogee capitol was taken over by the U.S. Government, the Creek Indian were able to establish a new capitol complex. This began with a push in 1971 to restore the abolished government of the Creek Nation. The new capitol remains in Okmulgee, only a short drive from the original.