Walsh told Collingwood staff and players on Wednesday of his decision to leave after seven years at the club.
He will continue in a consultancy role for his three-month notice period, with the day-to-day operations of the football department to be overseen by football and coaching strategist Rodney Eade.
Chief executive Gary Pert and national recruiting manager Derek Hine will take charge of player contracts. The pair have already been in contact with Paul Connors, the manager of uncontracted forward Dale Thomas.
Walsh said he was looking forward to an "extended break" during which he plans to visit the US with family.
Collingwood president Eddie McGuire said Walsh was an essential contributor to the club's 2010 premiership win.
"Geoff Walsh's contribution to the Collingwood Football Club has been profound," he said in a statement.
"He was one of the key architects of the rebuild of the team and our 2010 premiership success.
"He leaves the football department in great shape, which is a testimony to his professionalism and skill."
Walsh said it was time for him to move on from Collingwood.
"I’ve enjoyed the privilege of working for some great football clubs and Collingwood is certainly that," he said.
"I've got misgivings about leaving. Collingwood is a wonderful place to work.
"I've made some lifelong friends in my time and I’m certain that with Nathan and the many other good key people in place the club is preparing for another period of success.
"But it's the right time personally and professionally for an extended break. Simply, I thank Collingwood for the opportunity."
Pert said he didn’t expect Walsh's departure to affect the club's daily operations.
"Derek is across all the negotiations. So am I. Any of the other planning for next year, be it contracting other staff, organising training camps will be done by 'Rocket' (Eade), myself, Bucks (coach Nathan Buckley and (fitness coach) David Buttifant. You have lots of senior people there," he said.
And he said that now was as good a time as any for Walsh to move on.
"It might seem to people that the timing is a little bit strange, but there's no off-season. Now is the time for Geoff to say I'm going to let someone else make those decisions and put those plans into place."
Ben Guthrie covers Collingwood news for AFL Media. Follow him on Twitter: @AFL_BenGuthrie
