In a stunning reversal, the Tories saw their December 2019 general election majority of more than 24,000 votes overturned by the centrist Liberal Democrats in the Tiverton and Honiton constituency.
At the same time, the main Labour opposition regained the Westminster seat of Wakefield, in northern England, in a further sign of its resurgence following the party's worst electoral performance in decades two and a half years ago.
The disastrous outcomes for the Conservatives are set to pile new pressure on the embattled Johnson, as the highly damaging "Partygate" scandal involving lockdown-breaching gatherings in Downing Street continues to plague him and his party.
The latest in a string of electoral defeats for the Tories in the last year, the dire results spurred the immediate resignation of the party's chairman, Oliver Dowden.
"Our supporters are distressed and disappointed by recent events, and I share their feelings," the key Johnson ally wrote in a resignation letter to the Conservative leader.
"We cannot carry on with business as usual. Somebody must take responsibility and I have concluded that, in these circumstances, it would not be right for me to remain in office."
But Johnson, in Rwanda for a Commonwealth summit, insisted he would not step down.
"Clearly we've got to listen to these results," he told UK broadcasters accompanying him.
"We will keep going, addressing the concerns of people," Johnson added.
The votes were held Thursday after the two areas' former Tory MPs both resigned in disgrace in recent months.
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