During that time, the 92-year-old created a media empire spanning from Australia to the United States.
His son, Lachlan Murdoch will become the sole chairman of News Corp. and continue as the chair and CEO of Fox, the companies said on Thursday.
The transition solidifies Lachlan's role as the leader of the media empire, putting to rest questions of succession within the Murdoch family.
It comes just months after Murdoch scrapped a plan that would have reunited his media empire by merging Fox and News Corp.
Murdoch, who has near-controlling stakes in both companies, will be appointed chairman emeritus of both the companies.
In a memo to staff Thursday, he wrote: "Our companies are in robust health, as am I."
Murdoch has long wanted his children to succeed him.
His son James had been CEO of Twenty-First Century Fox prior to the company's decision to sell its film and television assets to Disney for $71.3 billion, a deal that closed in 2019.
James then channeled proceeds from the deal into a private investment firm, Lupa Systems. Lachlan was appointed CEO of the new Fox.
Upon Murdoch's death, his other children could challenge Lachlan's power.
Shares of Fox were up 2 percent in morning trading while News Corp stock rose about 1 percent.
