Popp was named general manager and director of player personnel of the CFL's Baltimore Stallions in 1994. After two Grey Cup appearances (including one championship), the team was forced out of Baltimore when the NFL started the Baltimore Ravens. Stallions owner Jim Speros decided to relocate his team to Montreal as the second incarnation of the Alouettes.
Popp stayed on as general manager, but found himself having to rebuild the team from almost nothing. While the Alouettes were allowed to reclaim the legacy of the original 1946-86 Alouettes, they were not allowed to keep their history as the Stallions. However, while all of the Stallions players were released from their contracts, Popp re-signed most of the key players from that team.
The Alouettes have been in eight Grey Cup Championships during Popp's tenure (2000, 2002, 2003, 2005, 2006, 2008, 2009 and 2010), capturing the title three times (2002, 2009 and 2010).
During the 2001 season, Popp took over the team after he and owner Robert Wetenhall fired Rod Rust in the midst of a long losing streak. On October 4, 2006, following the resignation of Don Matthews due to health reasons, Popp again took over as head coach and led the Alouettes to an appearance in the 2006 Grey Cup. Popp continued leading the Alouettes during the 2007 season as well, a rebuilding year which saw the team play with 23 rookies and without their starting quarterback for half the season. Following the 2007 season, Popp decided to step away from the coaching ranks when he hired former NFL coach Marc Trestman as the new head coach of the Alouettes. On August 1, 2013, Popp returned to the sideline after the firing of new head coach Dan Hawkins and was interim head coach for the remainder of the 2013 season. For 2014, Tom Higgins was hired as the Alouettes' head coach and Popp returned to general manager duties full-time. On August 21, 2015, Alouettes ownership relieved Tom Higgins of his coaching duties and brought general manager Popp to the bench for the fourth time. Jim Popp continued on as the head coach for the 2016 CFL season. The first 13 weeks of the season proved to be very tumultuous for the Al's both on the field and in the locker room. Jim Popp only managed to coach Montreal to victories in 3 of first 12 games before relinquishing his responsibilities as head coach to Jacques Chapdelaine who had been serving as a wide receivers coach and special assistant to the offensive coordinator.
Under Popp's guidance, his teams have reached the playoffs for 20 consecutive seasons, advancing to the Divisional Championship game 15 times. Popp's teams have appeared in 10 Grey Cup championship games, winning the Grey Cup four times.
Popp was successful in convincing the Argonauts ownership in hiring Marc Trestman as the team's head coach. Popp and Trestman won consecutive Grey Cups together in 2009 and 2010.
Despite being hired later during the free agency period, Popp was able to sign former Montreal Alouettes players Bear Woods, Jeff Perrett and S. J. Green. Popp was initially criticized for the moves by the Toronto media, as some felt he was turning the Argonauts into another version of the Alouettes.
Popp's first season in Toronto went above expectations, given the circumstances. The team finished the season at 9-9, which was good enough for first place in the East and a first-round bye in the playoffs. Under his leadership, the Argos defeated the Saskatchewan Roughriders in the Eastern Final, and the Calgary Stampeders in the 105th Grey Cup CFL final.
Popp's second season in Toronto went way below expectations. The team nosedived from winning the Grey Cup a year earlier to finishing the season at 4-14, with an 0-9 record on the road. The team struggled to find consistency at the quarterback position following a season-ending injury to Ricky Ray. Popp traded for James Franklin from the Edmonton Eskimos in the off-season, with the hopes of him being the successor to Ray. Franklin struggled to find his footing and would be replaced by McLeod Bethel-Thompson, who would also struggle at the helm. The team's on-field performance and nosedive in the standings prompted Popp to fire Trestman at the end of the season.
Popp and his wife Kimberly have six children and reside in Mooresville, North Carolina and North York, Ontario (during CFL season). Popp credits much of his success on the field to his family, especially his father Joe, a former NFL and college coach. Jim and his father share the privilege of being members of the Mooresville (NC) High School Hall of Fame, whose football stadium is named in Joe's honor (Coach Joe Popp Stadium).