Dimitroff was born in Ohio to Tom Dimitroff, Sr. and Helen (neé Kenhart). He grew up in Canada, where his father was a football coach with the Ottawa Rough Riders, Hamilton Tiger-Cats, and the University of Guelph in Ontario. In 1983, Dimitroff served as an equipment manager for the Guelph football team. From 1985–1990, he played defensive back for the Gryphons football team and was team captain from 1988–1990. Dimitroff graduated from Guelph with a Bachelor of Arts degree in 1990. His brother Randy played quarterback for Guelph from 1982–1985 and the two were teammates in 1985. His nephew Dillon Dimitroff also played for Guelph from 2009–2012.
After graduating from college, Dimitroff joined the Saskatchewan Roughriders of the Canadian Football League as their Canadian scouting coordinator, but worked in many areas of the team's operations for the two seasons he was there. In 1992, he worked in the Dallas, Texas office of the World League of American Football, tracking NFL player transactions and rosters. When the league folded later that year, Dimitroff moved to Japan, where he helped coach a friend's corporate American football team.
Dimitroff then considered leaving the football world for business, but instead he went back to the United States, where he joined the Cleveland Browns' grounds crew; his father was a scout for the team at the time. There he worked under then-head coach Bill Belichick and then-pro personnel assistant Scott Pioli. At the same time, he worked as a part-time scout for the Kansas City Chiefs in 1993. In 1994, Dimitroff became a full-time area scout for the Detroit Lions, a position he held through 1997. He then held a similar college scouting position with the Browns from 1998 through 2001.
In 2002, Dimitroff re-joined Belichick and Pioli with the New England Patriots as a national scout. He spent the season reporting on the nation's top prospects before being promoted to director of college scouting on June 11, 2003. He oversaw the team's college scouting operations through the 2007 season.
After six seasons with the Patriots, Dimitroff was hired as the Falcons' general manager on January 13, 2008.
In the 2008 NFL Draft, Dimitroff and the Falcons drafted both quarterback Matt Ryan and offensive tackle Sam Baker in the first round. The Falcons also signed free agent running back Michael Turner from the San Diego Chargers, who was selected to the 2009 Pro Bowl in his first year with the team. The Falcons, under first-year head coach Mike Smith, reached the playoffs in 2008 for the first time in four seasons, but lost to the Arizona Cardinals in the opening round. Soon after, Sporting News named Dimitroff their 2008 NFL Executive of the Year.
The Falcons finished 9–7 in 2009, missing the playoffs. In 2010, the Falcons finished 13–3, earning home field advantage for the duration of the playoffs; however, they lost to the Green Bay Packers in the Divisional round. He was named the 2010 NFL Executive of the Year by the Sporting News, his second time receiving the award. The Falcons then made consecutive playoff appearances in 2011 and 2012 with records of 10-6 and 13-3 respectively. The Falcons reached the NFC Championship game in 2012 and were four points away from the Super Bowl. After five successful seasons, the Falcons took a turn for the worse and generated records of 4-12, 6-10, and 8-8 the next three years. In 2016, the Falcons finished the regular season 11-5, and they earned a trip to the Super Bowl, winning the NFC Championship against the Packers. It was also the last game at the Georgia Dome.