After retiring as a player, Bowles was a member of the Green Bay Packers' player personnel staff from 1995–1996. He was the defensive coordinator and secondary coach at Morehouse College in 1997, and the defensive coordinator and defensive backs coach at Grambling State from 1998–1999. He was the defensive backs coach for the New York Jets in 2000, Cleveland Browns in 2004, and Dallas Cowboys from 2005–2007. He was the Browns' defensive nickel package coach from 2001–2003.
Bowles was hired by the Miami Dolphins as the team's secondary coach and assistant head coach on January 23, 2008. After nearly four seasons as the secondary coach and assistant head coach, he was named the interim head coach on December 12, 2011, following the firing of head coach Tony Sparano. Bowles' first game as interim head coach of the Dolphins came on December 18, on the road against the Buffalo Bills. The Dolphins won the game 30-23. The Dolphins finished 2–1 under Bowles in 2011.
The Philadelphia Eagles hired Bowles as the team's secondary coach on January 30, 2012. The Eagles announced on October 16, 2012 that they dismissed defensive coordinator Juan Castillo from his duties and named Todd Bowles as their new defensive coordinator. Under Bowles, the Eagles finished the season ninth in pass defense and twenty-third in rushing defense.
On January 18, 2013, Bowles was hired as defensive coordinator for the Arizona Cardinals. On January 31, 2015, he was voted Associated Press (AP)'s Assistant Coach of the Year for his efforts in the 2014 season. Bowles received 22 of the 50 media members' votes, winning the inaugural award.