Later in his career, Holmes studied at Harvard University's John F. Kennedy School of Government, receiving a Master of Public Administration in 2000.

After his clerkships, Holmes entered private practice with the law firm Steptoe & Johnson in its Washington, D.C. office.

Holmes wrote for a unanimous three-judge panel holding that a criminal defendant was improperly ordered to pay immediate restitution to the victim of his crime.

Holmes was on the first federal appellate court panel to weigh affirmatively on the constitutional right of same-sex couples to marry.

He penned an important concurrence on the role of animus in the ban of same-sex marriage in Oklahoma.