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Holmes was initially nominated for a federal judgeship in the United States District Court for the Northern District of Oklahoma, having been chosen from group of finalists that included Tulsa attorneys Lane Wilson and John M. O'Connor (Wilson would later serve as U.S. Magistrate Judge for the Northern District before leaving to become General Counsel at the Williams Companies). While his nomination for a United States District Court seat was pending, Holmes was nominated by President George W. Bush on May 4, 2006, to fill a seat vacated by Judge Stephanie Kulp Seymour. Bush's previous pick to replace Judge Seymour, United States District Judge James H. Payne, withdrew over criticism of his handling of cases in which he allegedly had a conflict of interest. The United States Senate confirmed his nomination less than three months later on July 26, 2006, by a 67–30 vote. He received his commission on August 9, 2006. He became the chief judge on October 1, 2022.
Notable cases
Holmes' first published opinion for the court, United States v. Ahidley, was released on May 25, 2007. 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.