During his time at Florida State, Bowden led FSU to an Associated Press and Coaches Poll National Title in 1993 and a BCS National Championship in 1999, as well as twelve Atlantic Coast Conference championships once FSU joined the conference in 1991. Bowden's Seminoles finished as an AP top-5 team for 14 consecutive seasons, setting a record that doubled the closest program. However, the program weakened during the mid-2000s, and after a difficult 2009 season Bowden was fired by President T.K. Wetherell, just weeks after his 80th birthday. He made his final coaching appearance in the 2010 Gator Bowl game on January 1, 2010, with a 33–21 victory over his former program, West Virginia.
Bowden spent the last part of his career in a race with Joe Paterno to become the winningest NCAA Division I college football coach of all time. The coaches overtook each other throughout the 2000s, sitting just a game apart before the 2008 college football season. However, on March 6, 2009, an NCAA ruling required Florida State to "vacate wins for any games in which an ineligible player participated", threatening to remove as many as fourteen of Bowden's wins from the 2006 and 2007 seasons in relation to an academic scandal. Florida State appealed the ruling, but the NCAA upheld it on January 5, 2010. Upon final investigation by FSU, it was determined that Bowden was to vacate 12 wins, bringing his final career record to 377–129–4, second to Paterno's final tally of 409 wins.