Fagan had been acting in the role for several months after the departure of James Fantasia in June, but has agreed to take the position on a permanent basis.
Part of the AFL industry for 15 years, Fagan joined the Hawks in 2008 as head of coaching and development.
Before that, he spent 10 years at Melbourne, starting as a development coach before becoming an assistant coach and later head of football.
Hawthorn CEO Stuart Fox said Fagan's appointment was a positive for the 2013 premiers.
"Chris has done an outstanding job stepping up to take on the responsibilities of [this role] in the interim, while maintaining some duties and tasks in his coaching role," Fox said in a statement on Tuesday.
"His experience has been invaluable to the department, and his work alongside the coaches, players and administration staff has been first-class in what has been a critical time in our season.
"We have always been aware of his remarkable work ethic, quality leadership skills and football intellect and we look forward to Chris leading our football department as the club continues to strive for sustained success."
Fagan's appointment follows Monday's announcement of four changes to Hawthorn's coaching panel, with Cameron Bruce promoted to assistant coach, replacing Adam Simpson, Adem Yze moving to a full-time specialist coaching role, Damian Carroll transitioning from Box Hill coach to head of Hawthorn's development academy, and Marco Bello taking over at Box Hill.