Private practice

After clerking, Hunt worked for five years at White & Case as an associate, and four years at King & Spalding, where he became a partner.^[1][2]

U.S. Department of Justice

In 1999, Hunt joined the United States Department of Justice Civil Division's Federal Programs branch, where he was a trial attorney until 2002. From 2001 to 2002, Hunt was detailed to the Office of the United States Deputy Attorney General. In 2002, Hunt became Director of the Federal Programs Branch.

After Jeff Sessions became United States Attorney General in February 2017, Hunt served as his chief of staff until October of that year. Hunt became a Senior Advisor to the Office of Legal Policy in October 2017, in which capacity he remained September 2018.^[1][2]

Assistant Attorney General

On September 14, 2017, President Donald Trump announced his intent to nominate Hunt to become the United States Assistant Attorney General for the Civil Division. Hunt's nomination was sent to the Senate on December 11, 2017.^[3]

The nomination was not acted upon, so on January 3, 2018, it was returned to the President under Rule XXXI, Paragraph 6 of the United States Senate.^[4] Hunt was renominated on January 8, 2018, and had a confirmation hearing on March 7, 2018, before the Senate Judiciary Committee.^[5] On April 19, 2018, Hunt's nomination was reported out of committee by an 18–3 vote.^[6] On August 28, 2018, the Senate voted to confirm him to head the Civil Division by a vote of 72–23.^[7] Hunt was sworn in on September 4, 2018. He oversaw the legal defense of Trump administration policies, as well as the general refusal to respond to Congressional oversight authority. Hunt declared that he would leave his position in early July 2020.^[8]

Samford University

On March 1, 2023, Hunt became general counsel of his alma mater, Samford University, in Birmingham, Alabama. He succeeded Clark Watson in the post.^[9]