He and Latics team-mate David Eyres took temporary charge of the Nationwide League Division 2 side for 12 matches after Iain Dowie departed for Crystal Palace.
However, John was back among the ranks when the Pilgrims lost 4-1 at Boundary Park in April on their way to the divisional title.
Having retired from playing at the end of that campaign, and taking charge of Oldham’s youth and, then, reserve teams, John began his management career proper back at Boundary Park in the summer of 2006, taking over from Ronnie Moore.
He guided the team into the Coca-Cola League 1 play-offs in his first season, after missing out on promotion by finishing sixth, with the Latics losing 5-2 to Blackpool in their two-leg semi-final.
Oldham finished eighth the following season but were unable to achieve promotion in John’s near three years at the helm.
However, his win-loss record (40%-31%) was very decent and he was unlucky to lose his job to the short-lived return of Joe Royle.
John bounced back immediately with League 2 Chesterfield and took them up as champions in his second season, 2010-11, the Spireites’ first at their new all-seater Proact Stadium.
After being promoted on a night off as Torquay and Wycombe drew, Chesterfield were confirmed as champions on the final day of the season when they beat play-off contenders Gillingham.
John was named npower Football League Two Manager of the Year for his achievements.
The task of keeping them in the third tier proved beyond him last term, although there was some compensation when the Spireites made it all the way to Wembley to lift the Johnstone’s Paint Trophy, beating Swindon 2-0 in the final.
John and Chesterfield parted company after just four winless games of the current campaign (two draws, one defeat), and he left with a win-loss record of 39%-37%.
Argyle visit Chesterfield’s 10,400 capacity Proact Stadium on Saturday, March 23.