I think a self-described agnostic or otherwise irreligious person would have a solid chance of winning the Democratic nomination so long as they were respectful of other peoples' faith (though they'd have a tough time forming the right combination of voters). They'd probably suffer an electoral penalty in the general election, but it would probably only be 1-2% at most. I don't think they could win the Republican nomination, though.
A self-described atheist in the style of Sam Harris or Richard Dawkins might have a shot at the Democratic nomination, but they'[woul]d get blown out in the general.
My thoughts exactly. They can't be condescending towards religious people.
And like the OP says, I don't think it can happen within the next 20 years or so. We might have to have a President Pete Buttigieg before we can have a President Kyrsten Sinema.