Marsh, who has been at the helm for 11 years, will replace Todd Greenberg as chief executive of the Australian Cricketers' Association.
His resignation comes mere weeks after Geelong captain Patrick Dangerfield stepped down as AFLPA president in favour of Collingwood skipper Darcy Moore.
Marsh was involved in multiple player collective bargaining agreement (CBA) negotiations with the AFL.
They included the 2017 AFL CBA, where players secured a percentage share of industry revenue for the first time, then a historic joint AFL-AFLW agreement six years later.
The 2023 agreement delivered AFL and AFLW players a 37.1 per cent share of industry revenue.
"I'm proud to have served the AFLPA and its members for nearly 11 years, and it's a role I've absolutely loved," Marsh said in a statement.
"It has been incredibly challenging but also rewarding and I trust I leave with the AFLPA in a better place than when I started.
"I make this decision with a heavy heart.
"... I am excited about the opportunities and challenges that are ahead at the Australian Cricketers' Association and am looking forward to getting started in June."
Moore hailed Marsh's impact during his time leading the players' union.
"Marshy has been a true player advocate and all current and past players have been extremely fortunate to have had him in our corner for as long as we have," he said in a statement.
Marsh, the son of Australian cricket legend Rod, previously led the ACA between 2005 and 2014.
"Paul has an unmatched depth of experience and expertise, having spent close to two decades at the head of Australia's leading player associations," ACA chair Greg Dyer said in a statement.
"Cricket is in his blood - his passion for our game and its players is obvious."
"We feel very fortunate to have attracted him back to cricket as we navigate significant change in the global landscape."
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