She served as the deputy whip from 2004 to 2006, vice chair of the Republican caucus from 2006 to 2008, and majority floor leader from 2014 to 2016.

[3] She was the first Native American, the first woman, and the first Chickasaw Nation citizen to represent her district.

[5] On December 21, 2017, the United States Senate confirmed her nomination by voice vote.

[citation needed] In January 2019, Governor Kevin Stitt appointed Billy to serve as the first Oklahoma Secretary of Native American Affairs.

She resigned in December 2019 citing the Stitt administration's conflict with tribal governments over gaming compacts in the state.