CEO Sam Haskell resigned from the Atlantic City-based organization on Saturday, a day after he was suspended by the board. Also on Saturday, President Josh Randle and Chairman Lynn Weidner resigned.
The organization announced the resignations a day after dozens of former Miss Americas signed a petition calling on the group's leadership to step down.
The emails were leaked to the Huffington Post, which first reported on them Thursday. Haskell said he made "a mistake of words."
"Those who know my heart know that this is not indicative of my character, nor is it indicative of my business acumen," Haskell wrote in a statement issued Friday.
Haskell's resignation is effective immediately, while Randle and Weidner will remain for a few weeks to help with a leadership transition. Dan Meyers, who had been vice chairman of the board, was named interim chairman.
In separate statements, the Miss America board confirmed the resignations of Randle, who became president in May and at 29 was the youngest to hold that position with the organization, as well as Haskell and Weidner.
The emails included one that used a vulgar term for female genitalia to refer to past Miss America winners, one that wished that a particular former Miss America had died and others that speculated about how many sex partners another former Miss America has had.
Several of the emails targeted Mallory Hagan, who won the 2013 pageant, claiming she had gained weight after winning and speculating about how many men she had sex with.
The emails already cost the pageant its television production partner and raised questions about the future of the nationally televised broadcast from Atlantic City's Boardwalk Hall the week after Labor Day each year. dick Clark productions told The Associated Press on Thursday that it cut ties with the Miss America Organization over the emails, calling them "appalling."
Also on Saturday, one of the main recipients of fundraising from the Miss America Organization said it is reviewing its association with Miss America. The Children's Miracle Network Hospitals said it was "conducting an immediate review of the situation and will take appropriate actions."
"We are appalled by the behavior reported in the media and add our voice to others demanding investigation, action and change," the group said in a statement.
