Capers attended Mount Union College in Alliance, Ohio where he played linebacker and safety. He began his coaching career as a graduate assistant at Kent State University and the University of Washington. Later he was an assistant coach at Hawaii, San Jose State, California, Tennessee and Ohio State. After a stint in the USFL, he began his NFL career as an assistant with the New Orleans Saints and was named defensive coordinator of the Pittsburgh Steelers in 1991, including a trip to the AFC Championship game in 1994. He remained with the Steelers until becoming head coach of the expansion Carolina Panthers in 1995. After 1995's 7-9 season, a record breaking mark for an expansion team, the Panthers went to the NFC Championship game in 1996. Continuing to spend against the salary cap, and eventually taking control of personnel matters in 1997, the Panthers went 7-9, followed by a dismal 4-12 season in 1998, at the end of which he was terminated.

After being let go from the Panthers, he served as an assistant with the Jacksonville Jaguars until becoming the head coach of the expansion Houston Texans on January 21, 2001. After starting out 4-12 (2002) and 5-11 (2003) in his first two seasons in Houston, the Texans posted a 7-9 mark in 2004.

Capers was known for his abilities as a defensive coach, and for his conservative play-calling on offense. Several TV announcers were known to predict Texans plays on occasion. He was also famous because he kept a 17 hour per day work schedule and sleeping just five hours per night, often on a couch in his office.

The Texans announced in 2005 following their dismal record of 2-14 (worst in NFL) that Capers would be fired January 2, 2006.

On January 23, 2006, the Miami Dolphins announced the hiring of Dom Capers as the team's defensive coordinator. There, he will also serve as assistant head coach under Nick Saban.