At Miami Norland High School, he played linebacker and was also a 185-pound pulling guard during his junior year. He was also a member of the track team, where he competed in the 100 meters with a personal best time of 10.7 seconds.
Smith was a member of the Dennis Erickson's 1989 and 1991 national-championship teams for the University of Miami. He played strongside linebacker, where along with teammates Jessie Armstead and Michael Barrow, formed arguably one of the greatest linebacking corps in college football history known as "The Bermuda Triangle".
He was a two-time All-American, the Big East Conference co-defensive player of the year as a junior and a Butkus Award finalist. Smith stayed five years at the University of Miami, the first as a red-shirted freshman under Jimmy Johnson, so he could get a complete education. He earned his master's degree in marketing after getting his undergraduate degree in business management. In 2006, he was inducted into the University of Miami Sports Hall of Fame.
Smith was selected in the second round of the 1993 NFL Draft by the Dallas Cowboys, becoming a starter at weakside linebacker and being named to the NFL All-rookie team after registering 93 tackles. He was one of the fastest linebackers in the league, extremely quick and versatile.
In 1995 Smith was a restricted free agent and the team gave him a one-year qualifying offer instead of a long term deal, so he sat out the first 7 games in a contract dispute, in order to avoid injury and be more marketable in free agency. He signed and played in the nine games that were needed for his contract to not be voided for that season. In 1996, he signed a one-year contract with the Cowboys.
Smith started all four of his seasons with the Cowboys, and had two 100-tackle years, including 117 tackles in 1996. He helped the Cowboys win Super Bowl XXVIII and Super Bowl XXX.
In the 1990s, the Cowboys organization felt they could find linebackers through the draft, without the need of paying a premium and adversely impacting the salary cap, so they allowed talented and productive players like Ken Norton Jr., Dixon Edwards, Robert Jones and Randall Godfrey, to leave via free agency, instead of signing them into long-term contracts. In 1997, after he became a free agent, the Cowboys replaced him by drafting Dexter Coakley.
Although he was looking for a multiyear deal, because that season many teams had salary cap problems, he was forced to sign a one-year contract with the Philadelphia Eagles. His time with the team was disappointing after suffering a sprained left ankle in training camp and torn ligaments in his right ankle during the regular season, that limited him to only 7 games. He was placed on the injured reserve list on November 19.
In 1998, he reunited with Dennis Erickson, signing a contract with the Seattle Seahawks where he played for two seasons. He was third on the team with 90 tackles in 1999, but was released after the season because of salary cap reasons.
In 2000, he signed a one-year deal with the New Orleans Saints and although he lacked the size, he became the starting middle linebacker at 235 pounds, using his quickness to rank second on the team with 113 tackles, he also added two interceptions (on returned for a touchdown), 21 passes defended and two sacks. He became a key contributor for the Saints' defense and the team's run to the NFC Western Division title. He was re-signed for four more years in 2001. After injuries limited him to only three games in 2004, he decided to retire at the end of the season.
Smith played in the NFL for 12 seasons, recording 24 quarterback sacks, 11 interceptions and 4 touchdowns. He never appeared in a Pro Bowl, but he is the only professional football player to earn two College Football National Championship rings (1989 and 1991) and two Super Bowl rings (1993 and 1995).
Smith now owns and operates a real estate investment/development company. Darrin is a member of The Fountain of Pembroke Pines (Pastor Wayne Lomax) where he heads the Athletes for Christ Bible Study Ministry. He is married to Kimberly Smith and the father of twins, a boy and a girl, Darrin and Darris Smith.