The 37-year-old, who won the 2013 title with Sydney Roosters and the 2016 grand final alongside Holmes and Townsend at the Sharks, has inked a two-year deal to work alongside head coach Todd Payten.
Maloney will join Justin Morgan and Ben Rauter in the Cowboys' assistant coaching ranks where he will specialise in working on the side's attack.
The creative playmaker retired from playing rugby league in May of this year after a stint as a player-coach in the French Elite One competition with Lezignan.
That was after two seasons and 42 games with UK Super League outfit Catalans, following his 247 NRL appearances with Melbourne, the Warriors, Roosters, Sharks and Penrith.
Maloney, who also played 14 games for NSW and three times for Australia, is renowned for his rugby league nous and ability to pick apart an opposition defence.
It is those qualities, along with his recent playing experience in the modern game, that attracted the Cowboys.
"We are excited at the prospect of the new dimension James will add to our program," Cowboys general manager of football Micheal Luck said.
"With an experienced assistant in Justin Morgan coming on board this year, we made the decision to target a younger coach with recent experience on the field to focus on our attack.
"We met with Jimmy in Townsville last week and we were impressed with how he presented and the ideas he had to improve our team.
"He will be an excellent sounding board for our spine, in particular our young halves in Tom Dearden, Tom Duffy and Jake Clifford."
The Cowboys will play their first games of 2024 in the NRL's Pre-Season Challenge in February against Brisbane in Mackay and Canberra in Queanbeyan.
The side, which finished a disappointing 11th in 2023, open the NRL regular season against the Dolphins at Suncorp Stadium.
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