Choctaw origin stories describe Nvnih Waiya, located in what is now Winston County, Mississippi, as the birthplace of Choctaw society. For thousands of years the ancestors of today's Choctaw people supported their families by farming and hunting. The communities they formed constantly changed and adapted through time. Moundville, built in part by the ancestors of today's Choctaws, grew into the second largest pre-contact settlement north of Mexico a few centuries before Europeans arrival.

Spanish conquistadors landed on the Gulf Coast in the early 1500s. For the next several decades ancestral Choctaw people and their neighbors intermittently faced waves of European diseases and Spanish military invasions. In part because of Choctaw military resistance the Spanish left and the Choctaw Homeland was not entered by large groups of Europeans again until the French came in the late 1600s. During the interim the Choctaws adopted many survivors from other local tribes.

Formal relations with the United States began in 1786. The Choctaw served as military allies of the U.S. in the War of 1812 and the Creek War. Soon after Choctaws requested missionaries and western schools to come to Choctaw land. By the 1820s many Choctaw had become wealthy in western terms.  The Treaty of Dancing Rabbit Creek in 1830 set up the removal of most Choctaw Indians to Oklahoma territory, a 500-mile journey through frozen forests and disease-stricken swamps. It is estimated that perhaps one-quarter of the people died on the trip.

The years of resettlement in Oklahoma were trying ones, but the Oklahoma Choctaw were determined to rise again and began laying the foundations for governance, adopting a new constitution in 1834 and building a council house at Nvnih Waiya, Oklahoma. It was here the first tribal council meeting was held in 1838. In 1897 the Dawes Commission negotiated the extinction of tribal governments, and most tribally owned lands were distributed among tribal members. Remaining lands were opened to white settlement.

Like many other tribes, Choctaws served in both World Wars with distinction, and Choctaw code talkers used the Choctaw language as a code to transmit vital battlefield information. Over the years, the Oklahoma Choctaw recovered their governance and economic footing, and are preserving their heritage and culture with events such as the annual Choctaw festival and sites such as the Choctaw Nation Museum housed in their capitol building built in 1884 in Tuskahoma.