It had the hallmarks of a dynasty in the making. When Ron DeSantis was asked in February whom he would like to see succeed him as Florida governor when he is termed out of office in 2027, his answer was unequivocal: his wife, Casey.

“There’s no question about it,” he told a press conference in Tampa.

“She’s someone who has the intestinal fortitude and the dedication of conservative principles that, you know, anything that we’ve accomplished, that she’d be able to take to the next level.”

Now, storm clouds are swirling as Florida’s glamorous first lady, a close political adviser to her husband as well as his loyal wife, ponders whether to throw her hat in the ring.

A political initiative she founded in 2021 to improve welfare provision has become mired in controversy over its charity wing’s failure to file required tax documents. There have also been probing questions from Florida Republicans over a “probably illegal” $10m donation from a legal settlement to the state that was secretly directed to the charity – some of which ended up in the hands of her husband’s political cronies.

It is a scandal that some observers believe has the potential to sink her possible candidacy for the November 2026 gubernatorial election before it even begins, or at least provoke some soul searching in the DeSantis camp about how and when to launch it.

“This is really her first test of negative publicity, and some negative attention in the media, and we’ll see ultimately how that plays out,” said Michael Binder, professor of political science and public administration at the University of North Florida.

“I don’t know that it’s a death knell for her candidacy. Rick Scott was a Medicare embezzler and it didn’t necessarily prevent him from not only winning a governor’s race twice, but getting elected to the Senate. So these things can pass.

“But that being said, none of this is great for her. And press like this is not great.”

Binder’s department conducted a February poll that showed Casey DeSantis with a 30% approval rate overall, rising to 57% among registered Republicans.

“She polled well a year-plus ago because she has some name recognition relative to the other candidates. I suspect eventually she’ll get into the race. But I certainly see this being a tougher race than probably both parties might think,” he said.

It is an unfamiliar position for Casey DeSantis, 44, one half of what some see as the fairytale couple of Florida politics since their Disney World wedding in 2009. A former television news reporter with a compelling story, including surviving breast cancer, she has been her husband’s chief cheerleader, confidante and campaigner.

She was at his side through his first election to Congress in 2012 and elevation to the governor’s mansion in Tallahassee six years later on the back of a tweeted endorsement from Donald Trump.

As recently as February, her own star was shining brightly, even as Florida’s Republican legislators began pushing back against Ron DeSantis’s handling of state affairs and agenda after six years as governor.

Donors were reportedly lining up to support her potential candidacy. Sources told NBC News that DeSantis saw his wife as a way to keep the governorship out of the hands of some of those with whom he has been recently feuding, including the agriculture commissioner, Wilton Simpson, and another former ally, the representative Byron Donalds.

Then came the hammer blow of Trump’s endorsement of Donalds, before an alleged “kiss the ring” breakfast visit in March by both Ron and Casey DeSantis to the president’s West Palm Beach golf club. That was quickly followed by the burgeoning charity scandal enveloping the Hope Florida Foundation, a non-profit supporting Casey DeSantis’s flagship initiative to reduce government funding for welfare programs and replace it with more community and corporate input.

The Tampa Bay Times discovered that the DeSantis administration secretly directed $10m to the charity from a $67m overbilling settlement last year between the state’s agency for health care administration (AHCA) and the Medicare operator Centene. The direction was in apparent contradiction of Florida law requiring such money to be paid into a trust or act as general revenue for state legislators to spend.

It was subsequently revealed that two organizations that received money from Hope Florida gave $5m each to political committees that supported Ron DeSantis’s ultimately successful efforts last November to defeat a ballot amendment calling for the legalization of recreational marijuana.

On Wednesday, the executive director of Hope Florida, Erik Dellenback, resigned, as the charity came under heightening scrutiny.

The scandal has angered some senior Florida Republicans, including the house speaker, Daniel Perez, and the state representative Alex Andrade.

Perez said it appeared DeSantis transferred the $10m to Hope Florida “in the dead of the night” and has threatened subpoenas to get answers; Andrade, chair of the house healthcare budget subcommittee, last week spent two hours questioning the DeSantis-appointed AHCA secretary, Shevaun Harris.

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“The reference to that $10m not being taxpayer dollars I find offensive,” he said, after Harris explained the money was a “donation” by Centene to Hope Florida on top of the settlement, and therefore exempt from state law.

Andrade said he believed the redirection of the money was a DeSantis “policy decision … that I believe was illegal”.

Harris, who was appointed in February, claimed she was “ambushed” at the meeting, and has denied that AHCA did anything wrong. Florida’s attorney general, James Uthmeier, said Hope Florida’s actions were legitimate.

On Monday, Ron DeSantis lashed out at his fellow Republicans, adding more heat to a feud that has been simmering since legislators shut down his immigration proposals in January, then launched an inquiry into the DeSantis administration’s spending habits.

“Shame on you in the Florida house and your terrible behavior in leadership,” DeSantis told a press conference in Kissimmee, reported by Florida Politics.

The outlet said the governor denounced “a lot of baseless attacks” and “manufactured smears against the first lady and the program that’s Hope Florida”.

The next steps for Casey DeSantis are uncertain, but some observers believe the controversy has ended any hope she had of becoming only the third woman, after Wyoming’s Nellie Tayloe Ross in 1925 and Alabama’s Lurleen Burns Wallace in 1967, to succeed her husband as a state governor.

“It’s clear, even at this point, that the Hope Florida scandal is going to kill her campaign in the cradle,” Peter Schorsch, publisher of Florida Politics, wrote in a post on X.

“She’s never gonna get back to the pristine starting point she needed to be at to run for governor.”

Frank Orlando, political science professor at St Leo University, said Casey DeSantis had essentially been caught up in the escalating dispute between her husband and state politicians, who are making hay from the Hope Florida situation.

“She’s been a relatively popular first lady of Florida, and my feeling from talking with legislators in Tallahassee is that it’s primarily a beef with Ron,” he said.

“It’s just finding ways to pick fights, to undermine his authority. To the extent that Casey is involved, it’s the fact that she would be in that wing of the party, and holding that banner. I don’t think this is being done to undermine Casey as much as it is saying to Ron: ‘We’ve been under your thumb for six years, and we’re not going to take it any more.’”

• This article was amended on 18 April 2025. An earlier version incorrectly stated Casey DeSantis would be the second woman to succeed her husband as a state governor, not the third.