Cullerton was in his third spell at the club, having returned at the start of the 2020/21 season.
He had previously left in the summer of 2019 to take up the manager’s role at Stone Old Alleynians, before being sacked three months in to the season despite Stone being third in the table.
Leek reached the play-offs in the NPL West Division this season, losing to Runcorn Linnets in the play-offs.
A Leek Town statement said: “The club would like to place on record their sincere thanks to him for his service over many seasons.
“Good luck Jamie, you will always be welcome at Harrison Park.”
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