In 1997, Jim Leavitt, previously the co-defensive coordinator at Kansas State, was hired as the team's first head coach.

[2] Their first team meeting was held under a shade tree, as the school had no proper football facilities on campus.

The Bulls' high ranking was short lived, as South Florida lost its next 3 games after injuries plagued the team.

Leavitt was fired on January 8, 2010, after an investigation revealed that, during halftime of a game against Louisville, he grabbed a player by the shoulder pads and struck him twice across the face.

[26] Following the regular season, he led the Bulls to 31–26 victory over the Clemson Tigers in the Meineke Car Care Bowl.

[28] To start the 2011 season, Skip Holtz led the Bulls to a dramatic 23–20 victory against Notre Dame, his alma mater.

[32][33] On December 8, 2012, USF announced the hire of Willie Taggart, who previously served as head football coach at Western Kentucky.

[40] The Bulls earned a bid to the Miami Beach Bowl against Taggart's former team and alma mater, Western Kentucky, a game USF lost by a score of 45–35.

The Bulls ended the 2016 season tied with Temple for 1st place in the East division, but because of a Week 8 loss to the Owls, USF did not play in the American Athletic Conference Championship Game.

In a Week 5 game against Cincinnati, Marlon Mack passed Andre Hall to become the leading rusher in program history.

In a Week 12 game against SMU, Quinton Flowers passed Matt Grothe to become the school leader in single-season total offense.

On November 30, 2016, Quniton Flowers was named the American Athletic Conference Offensive Player of the Year, which was the first such award in school history.

On December 7, 2016, Willie Taggart was announced as Oregon's new head coach, a position that was vacant after the firing of Mark Helfrich on November 29, 2016.

[44] Led by interim coach T. J. Weist, the Bulls ended their season with a 46–39 OT victory over South Carolina in the Birmingham Bowl on December 29, 2016.

With a 33–3 win over Cincinnati in Week 7, the Bulls extended their streak of 30-plus point games to 23, matching the AP Poll era record (since 1936) set by Oregon from 2011 to 2012.

[57] With a 34–28 win over Tulane in Week 8, the Bulls extended their streak of 30-plus point games to 24, setting the AP Poll era record.

During the Bulls' Week 13 game against rival UCF, Quinton Flowers passed Matt Grothe to become the program's all-time leader in total yards.

Despite the poor finish to the regular season, the Bulls were selected to play in the Bad Boy Mowers Gasparilla Bowl against Marshall.

[63] Scott was previously the co-offensive coordinator at Clemson, where he won the College Football Playoff national championship in 2016 and 2018, and made the final at the conclusion of the 2019 season.

On October 23, the team won their first game against an FBS opponent in the Jeff Scott era after beating Temple 34–14.

[68] South Florida fired Scott and defensive coordinator Bob Shoop on November 6, 2022, following a 1–8 start to the season.

[70] Golesh previously served as the offensive coordinator/tight ends coordinator for the University of Tennessee, where he was named a finalist for the Broyles Award after the 2022 regular season.

[74] The Bulls finished the 2024 regular season with a 6-6 record, and earned an invitation to the Hawaii Bowl to play San Jose State.

During the Week 8 game against UAB, wide receiver Sean Atkins passed Andre Davis for the most receptions in program history.

[82] † Interim head coach The Bulls played their home games at Tampa Stadium, which was also home of the Tampa Bay Buccaneers, during their debut season in 1997, as well as the first two games of the 1998 season before moving to the newly completed Raymond James Stadium.

In August 2017, USF officials announced they were exploring sites for an on-campus stadium that would seat 40,000 to 50,000 fans.

[83] In 2021, USF officials and the board of trustees expressed their renewed interest in an on-campus stadium making it a priority for the interim president Rhea Law.

[85] In September 2021, the university began construction on a luxury indoor practice facility, which was completed in November of 2022.

Known officially as the War on I–4, the intense rivalry with in-state opponent UCF began with a matchup in 2005 and has been played annually since 2013.

Under the current American Athletic Conference TV deal, all home and in-conference away USF football games air on one of the ESPN channels or are streamed on ESPN+.