The County legend has been on the staff at Edgeley Park since 2015, working as a scout initially before joining the coaching staff.
He worked under Neil Young before the return of Jim Gannon in January last year.
Flynn also took charge as caretaker-manager for the home draw with Nuneaton Town after Young resigned from the hot seat at Edgeley Park.
Manager Jim Gannon said: “We’re all sad to see Flynny leave the club but we understand that the opportunity to progress his career left him with a difficult choice to make.”
Flynn captained the Hatters through the glory years of the 1990s, playing alongside Gannon.
He made a club-record move from Preston to County in 1993 and went on to lead the Hatters into the second tier in 1997, as well as the League Cup semi-final.
Flynn then helped County punch above their weight in the Championship before relegation in 2002, two months after he had signed for Barnsley.
Flynn played 460 games for County, scoring 19 times, before returning to the club in 2015.
He will remain a club Life President.
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