Bobby Bowden served as an assistant football coach and head track and field coach at Howard College (now known as Samford University, currently in the FCS football division) in Birmingham, Alabama from 1954–55. He left his alma mater to become Athletic Director as well as head football, baseball, and basketball coach at South Georgia College from 1956 to 1958. Bowden then returned to Howard as head coach, where he compiled a 31–6 record between 1959 and 1962. In 1962, Bowden went to Florida State University as an assistant coach under Head Coach Bill Peterson. Two other coaching legends who worked under Coach Peterson during this time were Bill Parcells and Joe Gibbs. Bowden left Florida State in 1965 to go to West Virginia University as an assistant under Jim Carlen. When Carlen left following the 1969 season to become head coach at Texas Tech, Bowden replaced him. Bowden then compiled a 42–26 record at WVU before returning to FSU as head coach in 1976.

During Bowden’s first year as head coach at WVU, the football team of the state’s other top-division school, Marshall University, fell victim to a tragic plane crash. Bowden asked NCAA permission to wear Marshall jerseys and play Marshall’s final game of the 1970 season against Ohio, but was denied. In memory of the victims of the crash, Mountaineers players put green crosses and the initials “MU” on their helmets. Bowden allowed Marshall’s new head coach Jack Lengyel and his assistants access to game film and playbooks to acquaint themselves with the veer offense, a variation of the option offense which aids teams with weak offensive lines. Lengyel credits Bowden with helping the young Thundering Herd recover. Bowden reportedly became emotional while viewing the movie We Are Marshall, and has said that he was the original candidate for the Marshall head coaching job vacated by crash victim Rick Tolley.

Bowden became the head coach of the Florida State Seminoles because the climate was warmer than in Morgantown, and because Tallahassee was closer to Birmingham, Alabama, where his mother and mother-in-law both lived. The team had a 4–29 record over the previous three seasons, and Bowden planned to stay only briefly before taking a better job, perhaps as head coach at Alabama.

During his 34 years as Florida State’s head coach he had only one losing season–his first, in 1976–and declined head coaching job offers from Alabama, Auburn, LSU, and the National Football League’s Atlanta Falcons. From 1987 to 2000 the Seminoles finished every season with at least 10 wins and in the top 5 of the Associated Press College Football Poll, and won the national championship in 1993 and 1999.