As part of his departure, a new company, the McLaren Group, will be formed to hold both McLaren Automotive, the supercar maker, and McLaren Technology Group, which owns the racing team.
Bahrain's sovereign wealth fund, Bahrain Mumtalakat Holding Company, and the TAG Group will remain as McLaren's majority shareholders.
According to Autocar, Dennis will receive around 275 million pounds ($465 million) for his 25 per cent share in McLaren Technology Group, and his 11 per cent stake in McLaren Automotive.
The transaction will reportedly close within "the next days or months".
Above: Ron Dennis.
Dennis took charge of the struggling McLaren race team in 1980. Under his guidance, the team won 158 Grand Prix races, and 17 Formula One world championships.
The team also featured a cavalcade of renowned drivers, including Niki Lauda, Alain Prost, Ayrton Senna, Mika Hakkinen and Lewis Hamilton.
Above: McLaren MP4-12C.
In late 1980, McLaren employed fewer than 100 people, and was valued at around 3 million pounds ($5.1 million).
By the end of 2016, the McLaren group of companies employed 3400 people, and were valued at 2.4 billion pounds ($4.1 billion). Despite only being in existence for six years, McLaren Automotive has been profitable for the last four years.
Above: McLaren 570S Spider.
Dennis reportedly fell out with other shareholders in 2014 and was removed from positions of power within the companies in 2016. Neither party alluded to this in prepared statements issued overnight.
The businessman and former Formula One team principal said: "I am very pleased to have reached agreement with my fellow McLaren shareholders. It represents a fitting end to my time at McLaren, and will enable me to focus on my other interests.
"I have always said that my 37 years at Woking should be considered as a chapter in the McLaren book, and I wish McLaren every success as it takes the story forward."
Ron Dennis will now pursue his other business interests and consultancy work for businesses and government, as well as managing his family's Dreamchasing charity.
Above: McLaren F1.
Shaikh Mohammed bin Essa Al Khalifa, King of Bahrain and head of Bahrain Mumtalakat Holding Company, said: “There will be time in the near future to outline our plans, for the coming months and years will be an extremely exciting time in the story of McLaren.
"But now, today, it is appropriate that we pause to express our gratitude to Ron. So, on behalf of McLaren and all who sail in her, may I say three heartfelt words: thank you Ron.”