The investor's Penske Media Corp did not reveal terms of the deal but several media outlets including Variety, one of his titles, said the media company was spending $100 million for a controlling stake.
Wenner launched Rolling Stone in 1967 through a family loan when he was a hippie student in Berkeley, California. Within years he turned the magazine into a bible of rock music coverage and a platform for left-wing politics and experimental journalism by writers such as gonzo reporter Hunter S Thompson.
But even as Rolling Stone's reviews remain among the most closely watched in the music industry, the publication has struggled in an era when independent magazines find it difficult to stay afloat.
Rolling Stone suffered a major blow when it retracted a 2014 story about an alleged gang rape at the University of Virginia, with a review finding that the magazine ignored basic journalistic practices.
Penske said he hoped to ensure that Rolling Stone "continues to ascend for decades across multiple media platforms."
"Our interest in Rolling Stone is driven by its people, its cultural significance and the globally recognised brand that has no peer in its areas of influence," Penske said in a statement.
Wenner will move from serving as Rolling Stone's publisher to a new role of editorial director. Gus Wenner, Jann's son, will keep his position of president and chief operating officer of Wenner Media and join the advisory board of Penske Media Corp, the statement said.
Founded by Jay Penske in 2003, his company has amassed major titles in entertainment and culture including Variety, one of the most influential outlets in Hollywood, the lighter film site Deadline.com and the fashion business trend-settler Women's Wear Daily.