On February 20, 2017, Hunter was appointed Attorney General of Oklahoma to replace Scott Pruitt who resigned to become the Administrator of the Environmental Protection Agency.

Upon graduation Hunter entered private practice, specializing in energy, real property, public employment law and utility regulation.

From 1993 to 1994, Hunter served as the General Counsel of the Oklahoma Corporation Commission, the state's regulatory authority for public utilities, oil and gas, transportation and pipelines companies.

He also served as legal counsel to Congressman Watts in his work on the National Security and the Transportation and Infrastructure Committees.

[5] In August 2009, Democratic Governor of Oklahoma Brad Henry appointed Hunter the 47th Secretary of the Commissioners of the Land Office.

On February 17, 2017, Oklahoma Attorney General Scott Pruitt resigned to become Administrator of the Environmental Protection Agency under President Donald Trump.

[10] On May 26, 2021, five days after filing for divorce, Hunter announced he was resigning effective June 1 because "certain personal matters that are becoming public will become a distraction for this office".

[1] Early in his term as Attorney General, Hunter was named the chair of the Oklahoma Commission on Opioid Abuse, following the passage of Senate Concurrent Resolution 12.

[11] Hunter, along with legislative leaders and experts worked on a plan to intended to address the increases in addiction and overdoses from opioids.

[14][15] After the announcement, members of the Oklahoma state legislature raised concerns about the nature of the settlement, and the potential for it to circumvent the traditional legislative appropriations process.

[18] The case began trial in the summer of 2019, and gained national attention, as the potential ruling was thought to be an indicator of the prospects for other states and localities aiming to also address the opioid epidemic.

[23] In May 2020, Hunter filed lawsuits against three more opioid manufacturers (AmerisourceBergen Corp., Cardinal Health, and McKesson) in Bryan County District Court.

According to Health Crisis Alert, "According to the suits, in 2017, the three companies provided enough opioids to Bryan County that every adult resident there could have had 144 hydrocodone tablets.

She is a practicing lawyer who served as a member of the Oklahoma State Regents for Higher Education from 2000 to 2009, appointed by Governor Frank Keating.