Ayodele attended MacArthur High School in Irving, Texas, where he was named All-District as senior as a linebacker and tight end.
Although he had good grades in high school, he was missing a course to be able to accept the scholarship from Purdue University, so he enrolled at Coffeyville Community College for one year. He was switched to defensive end, registering 101 tackles, 7 sacks, 3 forced fumbles and 3 fumble recoveries. He received second-team NJCAA All-American, All-Jayhawk and Conference Defensive Player of the Year honors. At the time, he ranked second on the school all-time tackles for loss in a season (33).
Ayodele was a three-year starter at defensive end for Purdue University. As a sophomore, he recorded 64 tackles (19 for loss) and 11 sacks. The next year, he started the first 5 games at linebacker, registering 66 tackles (15 for loss), 9 sacks, 2 interceptions, 6 passes defensed and 2 fumble recoveries. He finished his career with 194 tackles (131 solo), 29 sacks, five fumble recoveries, four forced fumbles and 11 pass deflections. He was named the Jimmy Rogers, Jr. Most Valuable Lineman at the 2001 Wells Fargo Sun Bowl.
He was named first-team All-Big Ten Conference as a senior and second-team All-Conference as a sophomore and junior. He is tied with Jeff Zgonina for second on Purdue's career-record list with 29 sacks, topped only by Rosevelt Colvin with 33.
Ayodele was selected in the third round (89th overall) of the 2002 NFL draft by the Jacksonville Jaguars, with the intention of playing him at linebacker. As a rookie, he recorded 3 starts, 108 tackles (fourth on team), 3 sacks, 3 passes defensed, one interception, 2 forced fumbles and 13 special teams tackles (tied for second on the team).
He became a starter at outside linebacker in his second season, while posting 150 tackles (second on the team), one sack, 4 passes defensed, 2 interceptions and 3 fumble recoveries.
In 2004, he registered 131 tackles (second on the team), 2 sacks, 3 passes defensed, one forced fumble, one fumble recovery and one blocked field goal. The next year, he tallied 100 tackles and 4 forced fumbles (led the team).
Ayodele never missed a game and was the first player in franchise history to record at least 100 tackles in four consecutive seasons.
In 2006, he signed a five-year contract with the Dallas Cowboys as a free agent, to play inside linebacker in the team's 3-4 defense and help shore up their run defense. Coincidentally, as a child growing up in Irving, Ayodele was a ball boy for the Cowboys. In his first year, he recorded 84 tackles, 2 interceptions (third on the team), 4 passes defensed and 2 fumble recoveries.
In 2007, Ayodele had a chance to play on the same team with his brother Remi, while posting 95 tackles (fourth on the team), 2 passes defensed and 3 special teams tackles. After the team signed free agent Zach Thomas, he became tradable. On April 25, 2008, Ayodele was traded along with tight end Anthony Fasano to the Miami Dolphins in exchange for a fourth-round pick (#100-Tyvon Branch) in the 2008 NFL Draft.
With the Miami Dolphins he reunited with former Cowboys head coach Bill Parcells, who was the team's Executive Vice President of Football Operations. In 2008, he tallied 13 starts, 2 interceptions and one fumble recovery. The next year, he recorded 70 tackles (third on the team), one forced fumble and 2 fumble recoveries. He was released on March 5, 2010.
Ayodele signed with the Denver Broncos on April 24, 2010. He was assigned number 51 and released on August 24.
On September 10, 2010, the Buffalo Bills signed Ayodele to take the spot of LB Kawika Mitchell after the team placed him on the injured reserve list. He switched to number 50, appeared in 15 games (10 starts) and wasn't re-signed at the end of the season.
"Akin" is a short name for "Akinola", which in Yoruba language means 'the brave and wealthy one'. His younger brother Remi Ayodele played defensive tackle in the NFL.