Following graduation from Illinois, Oakes was named the football line coach at the University of Tennessee under head coach M. B. Banks. In 1926, Oakes was named the line coach at the University of Nebraska–Lincoln under Ernest Bearg and later worked under Dana X. Bible. Oakes's first head coaching assignment came in 1931 when he was named as the head football coach at the University of Montana. During his tenure at Montana, Oakes wrote and had published his book, Football Line Play. The book quickly became an important text for coaches and players throughout the country. It was also during this period in his coaching career that he received several patents for football blocking equipment. His dummies were the earliest mobile blocking equipment available to schools and enabled various formations to be simulated. In 1934, Oakes was named the head football coach at the University of Colorado at Boulder. His teams at Colorado won Rocky Mountain Conference titles during the 1935 and 1937 seasons. The 1937 team, which featured All-Americanhalfback and future justice of the Supreme Court of the United StatesByron White, went undefeated in the regular season and played in the 1938 Cotton Bowl Classic, the first bowl game appearance for Colorado. The 1939 Colorado team placed first in the Mountain States Conference. Oakes's record for the five years at Colorado was 25–15–1 with a conference mark of 24–6–1. Oakes returned to the University of Illinois in 1940, where he earned a Master of Science degree. In April 1941, Oakes took over as the head football coach at the University of Wyoming. With the onset of World War II, intercollegiate athletics were suspended in 1943 and Oakes concentrated on physical training of Army and Navy cadets at the University of Wyoming. Following the war, Oakes resumed his position as head coach for the 1946 season. Oakes completed his collegiate football coaching career at Grinnell College in Grinnell, Iowa. Assuming duties as head football coach and athletic director at Grinnell in 1947, Oakes completed his coaching career following the 1948 season.
Death and memorial
Oakes died on October 22, 1970 near Lancaster, Pennsylvania of an apparent heart attack while vacationing with his wife. At the 65th Annual Convention of the National Collegiate Athletic Association on January 11, 1971, a memorial resolution commemorating Oakes's distinguished service to athletics was adopted. The Memorial Resolution reads: "For his faithful service to his institution and higher education; his valuable contributions to intercollegiate athletics, and his wholesome influence upon the lives of young men. Be it known that the membership of the National Collegiate Athletic Association, assembled in annual Convention, resolved that this memorial be inscribed in honor and fond remembrance of Bernard F. Oakes."