The decision comes three weeks after the NHL said Bowman and two other Blackhawks executives were eligible to seek employment in the league again more than two years after they were punished in the fallout from the Chicago team's sexual assault scandal.
"I believe his vast experience and proven success in this role, together with the important work he has done in his time away from the game, fits our goal of being best in class when it comes to all facets of our organization," Oilers CEO of Hockey Operations Jeff Jackson said in a news release.
"Through our many conversations, we share a common vision of where we are as a team and what is required to achieve another Stanley Cup title."
Bowman, former Chicago coach Joel Quenneville and executive Al MacIsaac had been ineligible since October 2021 due to what the NHL called their inadequate response upon being informed in 2010 of allegations that one of their players had been assaulted by the club's video coach.
An investigation commissioned by the Blackhawks in 2021 concluded team officials mishandled allegations raised in 2010 by then-player Kyle Beach during the team's Stanley Cup run.
Following the report, Bowman and MacIsaac stepped aside from their roles with the Blackhawks while Quenneville, who had since moved on to coach the Florida Panthers, resigned from that position after meeting with NHL Commissioner Gary Bettman.
"My response was inadequate back in 2010," Bowman told reporters at his introductory press conference.
"I didn't handle things properly. I should have done more, and that's something I regret and that's something that I've had a chance to reflect on and try to learn from."