The executive will assume both the CEO and chairman jobs at the company, which is being referred to as New Fox.
James Murdoch, Lachlan's 45-year-old brother, now helms Fox.
The deal with Disney, which was announced in December, will see Disney acquire assets such as European satellite TV company Sky, the Twentieth Century Fox film and TV studios, cable network FX, Indian satellite group Star India and a stake in streaming service Hulu. But the matter may not be settled.
However, Comcast is widely expected to launch its own rival bid for Fox assets this summer, which could jeopardise the Disney agreement. He's expected to move on after the deal with Disney is completed, pursuing his interests in areas such as technology investments.
The new Fox will consist of the Fox News Channel, which is the top-rated cable news channel in the country, as well as the Fox Business Network and the Fox Broadcasting Company.
Disney would acquire Fox's film and television studios, its FX and National Geographic cable networks, Fox's regional sports networks, its stakes Hulu and in United Kingdom pay TV provider Sky, as well as Star India. The future of his vast holdings has been a source of longstanding debate within the industry.
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Prior to the Disney bid Fox had made an approach to acquire the 59 per cent of Sky it did not already own, however that deal has been repeatedly held up by United Kingdom regulators over fears it would undermine media plurality.
"We have worked through the winter "standing up" a reimagined independent Fox". The 46-year-old previously served as co-chairman and has been chairman of TV stations under its umbrella, as well as publisher of the New York Post.
According to the announcement, Fox chief financial officer John Nallen will take on the role of chief operating officer as a result of the transaction.
Another possible wild card for Fox is an attempt to buy the portion of United Kingdom satellite broadcaster Sky that it doesn't already own.
A late challenge has come from Comcast, the largest USA cable network, which is understood to have met with financiers in preparation for a $60 billion all-cash bid for Fox's entertainment package.