Cahill, a Football Development Ambassador for the organisation, presented the check to founder John Moriarty himself prior to Tuesday night's 3-0 victory over Lebanon.
As the nation's first Indigenous Socceroo, Moriarty founded JMF in order to train and teach aspiring young players currently residing in remote Northern Territory.
The sizeable donation from Australia's all-time leading goalscorer will allow JMF to continue its positive and fruitful engagement with the indigenous population of Australia, and Moriarty thanked Cahill and co. for their collective contribution.
"This wonderful donation from the Socceroos and Matildas is a remarkable gesture of goodwill and inclusivity," Moriarty said.
"It underlines the leadership our national women’s and men’s teams are showing in relation to Indigenous opportunity through football.
"Our whole Moriarty Foundation team thanks them and the PFA for their tremendous support.
"Many of our children in remote Northern Territory and on scholarship in Sydney will benefit.
"We also wish Tim Cahill and his family all the very best for the future, acknowledge his phenomenal contribution to the sport, and thank him warmly for his personal championing of John Moriarty Football."
38-year-old Cahill came on in the 82nd-minute with Graham Arnold's men leading Lebanon 3-0 in front of over 30,000 fans courtesy of a Martin Boyle brace and a second-half Mathew Leckie goal.