“I said, ‘Now, Andrew, go out and win this damn thing,’” she said. “Because this is too important.”

Mr. Gillum’s unexpected nomination represents a sharp break with recent Florida midterm elections in which Democratic voters nominated somewhat bland moderates to try to win in a purple state. Instead, they lost over and over again: Democrats have not held the Florida governor’s mansion in two decades, and they lost the past two governor’s elections by a single percentage point.

Mr. Gillum argued Democrats needed to back a progressive who could expand the electorate by attracting more black, Latino and millennial voters who might otherwise sit out the midterm.

“We’re showing that we can bring together the Bernie Sanders wing of the party and the Hillary Clinton wing of the party,” he said in a recent interview. Democrats cannot win, he added by “trying to be Republican-lite.”

Florida Democrats have long considered Mr. Gillum a rising star in a state party with few of them. He was elected to the city commission while still a student at Florida A&M University, and he spoke at the 2016 Democratic National Convention in Philadelphia.

But only in the last few weeks of the governor’s race did Mr. Gillum start looking like a serious contender. Early on, he struggled to raise serious money, as donors worried about an F.B.I. investigation into City Hall corruption — an inquiry that Mr. DeSantis wasted no time in raising Tuesday night. “He’s embroiled in corruption scandals,” the Republican said. “This guy can’t even run the city of Tallahassee.”

The mayor, who has said he is not the investigation’s target, consistently placed fourth out of five in public polls, despite outperforming his opponents in debates with his charisma on stage and grass-roots support in the audience.

His poor showing in surveys, however, kept his rivals from attacking him, allowing Mr. Gillum to move up unscathed by the pointed television attacks that engulfed Ms. Graham, Mr. Levine and Mr. Greene, a billionaire Palm Beach real estate investor who spent nearly $40 million but finished fourth.