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Republican Glenn Youngkin has a commanding lead in the Virginia governor's election, widely seen as a referendum on Joe Biden's presidency.
Democrat Terry McAuliffe, who served as governor from 2014-18, saw his opinion poll lead vanish in recent weeks.
A Democratic loss in a state that Mr Biden won by 10 points just a year ago would unnerve his governing party.
Mr Youngkin, a political newcomer, focused on how schools handle race, gender and mask mandates.
Mr McAuliffe campaigned on other cultural issues, such as abortion rights and voting reform.
But the Democrat's critics hammered him for saying during a debate: "I don't think parents should be telling schools what they should teach."
According to exit polls by the BBC's US partner, CBS, education and the school curriculum were top issues for slightly more than half of all voters.
At a news conference earlier on Tuesday, Mr Biden predicted his party would win the first major election since he took office 10 months ago, but he acknowledged "the off-year is always unpredictable".
Mr Biden's popularity has been sliding amid rising inflation, a slow economic recovery, a deadlocked legislative agenda and the aftermath of a disorderly US withdrawal from Afghanistan.
The Democratic president's approval rating has fallen to 43%, according to an opinion poll average by RealClearPolitics.
The McAuliffe campaign tried to liken the challenger to former President Donald Trump, who remains unpopular in Virginia.
But Mr Youngkin, a mild-mannered private equity tycoon, sought to appeal to moderates by keeping Mr Trump at arm's length, while tapping into the former president's supporters in the state.
Mr Trump reiterated his support for Mr Youngkin in a statement on Monday, saying: "He has had my complete and total endorsement for many months!"
The winner will succeed outgoing Democratic Governor Ralph Northam.
In other elections across the US on Tuesday:
- New Jersey's Democratic Governor Phil Murphy is trying to win a second term
- Minneapolis voters are deciding whether to replace their police department in the city where George Floyd was murdered by an officer
- Former police officer Eric Adams is expected to win New York City's mayoral election to replace Democratic Mayor Bill de Blasio
- In other mayoral races, voters in Boston were choosing between two women of colour, the first time the Massachusetts city will be represented by someone other than a white man