The team announced the move Thursday, saying Jackson will report directly to owner Daryl Katz and work closely with president of hockey operations Ken Holland. Katz called it a big commitment to the organization's long-term success.
"He brings tremendous industry insight, knowledge and leadership built through a unique career experience that is ideal for this leadership role," Katz said in a statement. "He understands what it takes to build an elite organization for the modern NHL and will work closely with Ken and our whole team to put the Oilers in the best possible position to win."
McDavid, the NHL's reigning MVP who's widely considered the best hockey player in the world, has three years left on his contract.
"Jeff and I have had a long, fruitful relationship," McDavid said. "I have witnessed his care, relentlessness and obvious knowledge of the game and industry firsthand. I look forward to working with Jeff in his new role and am excited about what this means for the future of the Oilers."
Jackson, 58, practiced law after his hockey playing career and spent time with the Maple Leafs before opening his own agency in 2010.
"I can't think of a more exciting franchise to join or a better opportunity for me to put into practice everything I have learned during the past three decades in and around the NHL," Jackson said. "I am very appreciative of the opportunity to help lead such a storied NHL franchise."
Hockey Hall of Famer and former Edmonton defenseman Paul Coffey will assist Jackson in his new role.