In 1943 he joined the U.S. Navy, where he was an assistant to Don Faurot with the Iowa Pre-Flight Seahawks football team and served as a hangar deck officer on an aircraft carrier. Following World War II, new Oklahoma head coach Jim Tatum persuaded Wilkinson to join his staff in 1946. (In fact, the OU Board of Regents stipulated that Tatum make Wilkinson his top assistant, or else their offer was null and void.) After one season in Norman, Tatum left the Sooners before the 1947 season for Maryland. The 31-year-old Wilkinson was named head coach of the Sooners (and athletic director) and would soon make history.
The centerpiece of his time in Norman was a 47-game winning streak from 1953 to 1957, an NCAA Division I record that still stands today and has only been seriously threatened thrice: by Toledo (35 wins, 1969-71), Miami (Fl.) (34 wins, 2000-03) and USC (34 wins, 2003-05). Earlier, the Sooners ran off 31 consecutive wins from 1948 to 1950. Except for two losses in 1951, the Wilkinson-coached Sooners did not lose more than one game per season for 11 years from 1948 to 1958, going 107-8-2 over that period. His teams also went 12 consecutive seasons (1947-58) without a loss in conference play — a streak which has never been seriously threatened. Wilkinson did not suffer his first conference loss until Halloween 1959 — his 79th conference game at Oklahoma.
His 1955 Oklahoma team is considered one of the greatest teams in college football history, regardless of era. He was also the first collegiate football coach to host a television show, aptly named "The Bud Wilkinson Show."
Wilkinson was also remarkable for compiling this record while showing a genuine interest and concern for the performance of his players in the classroom. Following the 1963 season, his 17th at Oklahoma, Wilkinson retired from coaching at the young age of 47.
While still at Oklahoma, Wilkinson served on the President's Council on Physical Fitness from 1961 to 1964, by which time he'd left the Sooners.
In 1965, Wilkinson joined ABC Sports as their lead color commentator on college football telecasts (teaming with Chris Schenkel and, later, Keith Jackson). Wilkinson was the color analyst for three of the greatest games in college football history: Notre Dame vs. Michigan State in 1966; Texas vs. Arkansas in 1969, and "The Game of the Century" Nebraska vs. University of Oklahoma in 1971. Wilkinson is still considered one of the best color commentators of all time because of his solid analysis and in-depth insight.
He was inducted into the College Football Hall of Fame in 1969.
Wilkinson was married to the former Mary Schifflet in 1938, with whom he had two sons. They divorced in 1975. A year later, he married Donna O'Donnahue.