Lockyer retired just days after the Magpies' premiership win for which he was an emergency.
The former West Australian played 227 games for Collingwood but hung up his boots after playing 11 senior matches in 2010.
He will take over the role of VFL coach from Gavin Brown, who earlier this month left the Pies to assume an assistant coaching position at Carlton.
"I'm thrilled that Collingwood has given me an opportunity to join the coaching panel and lead the VFL team," Lockyer told collingwoodfc.com.au.
"To coach within a structure I'm familiar with, and alongside some great people, is extremely exciting.
"I'm very thankful that the club I love and have a great history with has given me this opportunity to make the transition from playing to coaching. I can't wait to start this new phase of my life."
Collingwood football manager Geoff Walsh said the club was thrilled to have finalised its coaching structure ahead of next season.
The Pies lost three members from its coaching panel this season, with opposition analyst Paul Hudson (St Kilda) and Luke Beveridge joining Brown on the list of departures.
Earlier this week the Pies announced Craig McRae and Matthew Lappin had joined the coaching panel, with Lockyer topping off a new-look team.
In addition to his role as VFL coach, Lockyer will also work as a development coach under McRae, who has been appointed as development manager.
"To add someone of Tarkyn's calibre to our coaching structure is a huge positive for Collingwood," Walsh said.
"There is an enormous amount of admiration and respect for Tarkyn at our club and we have no doubt that he will thrive as VFL coach and development coach after a wonderful playing career."
