Felton got his start in the coaching profession as an assistant basketball coach at Oxon Hill High School in 1984. He then became an assistant coach at Charles County Community College, for one season before moving on to University of Delaware as an assistant coach for four seasons. Felton continued his collegiate career with one season each at Tulane University and St. Joseph's University. In 1992, he took an assistant's post at Providence College under Rick Barnes. That season began a 6-year apprenticeship with Barnes that included two with the Friars and four at Clemson University. The six teams that Barnes and Felton coached together all posted winning seasons, all played in the postseason and went 114–71, averaging 19 wins per year.
Western Kentucky
In the spring of 1998, just before Barnes left Clemson for Texas, Felton was named the head coach at Western Kentucky University. His first two Hilltopper squads went a combined 24–34. The 1999 team advanced to the Sun Belt Tournament title game. His Hilltopper teams won the Sun Belt Conference tournament titles in 2001, 2002, and 2003.
Georgia
In April 2003 Felton was hired as the head coach at the University of Georgia. Felton also took assistant coaches Bert Tucker and Ken McDonald as well as associate head coachPete Herrmann with him to Athens. In his first four seasons at Georgia, Felton had compiled a 58–63 record with two NIT appearances while attempting to lead Georgia back from the severe disadvantages that previous coach Jim Harrick dealt the program. Despite having only 9 scholarship players in 2007–2008, Felton's Bulldogs completed a successful run in SEC Tournament Championship history. Entering the 2008 SEC Men's Basketball Tournament as the lowest seed, Georgia to capture the conference tournament crown and the corresponding automatic berth in the 2008 NCAA Men's Basketball Tournament. In their first NCAA Tournament appearance since 2002, the Bulldogs were defeated by Xavier University in the first round in Washington, D.C.. On January 29, 2009, Dennis Felton was fired as head coach of the UGA Men's Basketball team. This came with a losing streak that left the team with a 9–11 record in mid-season He finished his career as the coach of UGA Men's Basketball team with an 84–91 record. Associate Head Coach Pete Herrmann finished the 2008–2009 season as the interim head coach.
Tulsa
Felton returned to college coaching after stints in the NBA, as an assistant coach on Frank Haith's staff at Tulsa.
Cleveland State
On March 24, 2017, Felton was hired as the head coach of Cleveland State University. On March 27, 2017 Felton was officially introduced as head coach. Felton's contract was for five years. On July 12, 2019, he was fired, along with his entire coaching staff.
Fordham
In 2019, Felton was hired as an assistant coach at Fordham University.
NBA coaching career
During the 2009–2010 NBA season, Felton served on the scouting staff for the Phoenix Suns, mainly observing NCAA games in the Southeast. He was also a part of the Suns' war room during the NBA draft in June 2010, led by General Manager Steve Kerr and head coach Alvin Gentry. On June 28, 2010, the New Jersey Nets announced that Felton would be an assistant coach for their Summer League team. Prior to the start of the 2010–2011 NBA season, he was hired by the San Antonio Spurs as Director of Pro Player Personnel, a position he held through 2013.
Head coaching record
Personal
Felton is married to the former Melanie Smith, who is also a Howard alumna. The couple reside in Milton, Georgia with their two sons, Jazz and Nile. Jazz and Nile are both basketball players. Jazz was a part of Milton High School's state championship team as a freshman in 2009–2010. Jazz will attend WKU and will serve on Ray Harper's coaching staff.