He served as general manager in the National Football League (NFL) for the Tampa Bay Buccaneers from 2004 to 2008 and the Washington Redskins from 2010 to 2019.

In his junior season, he ranked 16th nationally and broke the school record for punting, averaging 42.9 yards a kick; those numbers resulted in him being named to that year's All-ECAC and All-South Independent teams.

He joined the Oakland Raiders organization as a senior executive in 1995, specializing in salary cap management and free agency negotiations.

Following the 2003 season, the Tampa Bay Buccaneers gave general manager Rich McKay permission to leave the team as his relationship with Super Bowl XXXVII-winning coach Jon Gruden had deteriorated.

Shortly after Allen joined the Redskins, Jim Zorn and his staff were fired, allowing Mike Shanahan to be hired as head coach and executive vice president of football operations.

While Shanahan had the final say in football decisions, he and Allen split the duties of general manager, working in an arrangement similar to how Bill Belichick and Scott Pioli operated with the New England Patriots at the time.

[14][15] While general manager, Allen attempted to bridge the connection between the modern Redskins and the glory years of past, include hosting golf tournaments with former players and coaches, to bringing back the gold pants that his father's team had used in the 1970s.

[19] Allen's tenure with the team was met with heavy criticism and disapproval, with a popular "FireBruceAllen" hashtag campaign being used on social media throughout the latter half of the 2010s, before he was fired following a 3–13 season in 2019.