Fox Corporation’s chief legal officer, Viet Dinh, will depart at the end of the year, in a major shake-up at the company after the landmark $787.5 million settlement it paid to Dominion Voting Systems in April.

Mr. Dinh, a former official in the George W. Bush White House who amassed considerable power inside Fox, will advise the company after his exit, Fox said in an announcement on Friday.

Mr. Dinh gave what some inside the company considered flawed advice during the Dominion suit, which exposed a pattern of deceptive coverage by Fox News after the 2020 presidential election. He insisted that Fox was on firm legal footing and could take the case, if need be, all the way to the Supreme Court, where he believed the company would prevail on First Amendment grounds.

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Mr. Dinh’s departure raises questions about how Fox will handle the major lawsuits it still faces for airing false claims about widespread election fraud after the 2020 election. Another elections technology company, Smartmatic, has sued Fox for $2.7 billion. And Ray Epps, the man at the center of a widespread conspiracy theory about the attack on the U.S. Capitol on Jan. 6, 2021, filed a defamation suit against Fox last month.

The company also faces two shareholder lawsuits related to its coverage and the handling of the lawsuits.

The Dominion lawsuit has been destabilizing for Fox and the family that controls it, the Murdochs. The fallout is posing the most significant challenges the company has faced since allegations more than a decade ago that journalists employed by its British newspaper division were hacking into the voice mail accounts of celebrities.