The Liberal Democrats handed Boris Johnson the biggest by-election defeat in British history as the Tories lost a huge majority in Tiverton and Honiton and surrendered Wakefield to Labour on the same night.
Moments after the results were declared, Oliver Dowden, the Conservative Party co-chairman, resigned, plunging the Prime Minister's leadership into a deeper crisis.
In a letter to Mr Johnson published early on Friday morning, Mr Dowden said Tory supporters were "distressed and disappointed" and "I share their feelings".
Mr Dowden said he was quitting because "someone needs to take responsibility", adding: "We cannot continue with business as usual."
My letter of resignation to the Prime Minister. pic.twitter.com/xd5MtM2o3n
— Oliver Dowden (@OliverDowden) June 24, 2022
The Prime Minister said he would "listen" to voters but would "keep going" in the job, despite the humiliating double defeat.
Sir Keir Starmer, the Labour leader, said his party's victory in Wakefield showed the Conservatives were "out of touch and out of ideas".
Mr Johnson's leadership has been rocked while he is out of the country, with the Prime Minister currently in Rwanda as he attends the Commonwealth Heads of Government Meeting. The resignation of Mr Dowden will inevitably spark speculation on whether other senior Tory figures could quit.
The last time a government lost two by-elections on the same night was more than 30 years ago when Sir John Major was the Prime Minister.
The loss in Tiverton is particularly humiliating for the Prime Minister as it is the biggest ever majority to be overturned in a UK by-election. The record was held by Labour, which toppled a 23,927 Tory majority in Liverpool Wavertree in 1935.
On a balmy night in south Devon, Lib Dem candidate Richard Foord, a former army major, wiped out a colossal 24,239 majority to win a seat the Tories had held ever since its creation in 1997.
The result also surpasses the Lib Dems’ previous best showing, which came last year when they claimed North Shropshire, which the Conservatives had held by 22,949.
In Wakefield, the Tories lost a 'Red Wall' seat they had taken from Labour in 2019 in a comfortable victory for Sir Keir Starmer's party.
'Shockwave through British politics'
Mr Foord ended up with 22,537 votes after widespread tactical voting saw Labour, which came runner-up at the last election, lose its deposit.
In his victory speech Mr Foord said the result would “send a shockwave through British politics”.
To loud cheers he said: “Tonight, the people of Tiverton and Honiton have spoken for Britain. They’ve sent a loud and clear message: It’s time for Boris Johnson to go. And go now.
“Every day Boris Johnson clings to office, he brings further shame, chaos and neglect. Communities like ours are on their knees.
“I also have a simple message for those Conservative MPs propping up this failing Prime Minister: The Liberal Democrats are coming.”
Conservative candidate Helen Hurford, whose defence of the constituency was blighted by the fallout from the partygate scandal, got 16,393 votes.
Turnout was 52.3 per cent – which is high for a by-election – with 42,707 ballots being cast.
It was called when incumbent Conservative MP Neil Parish resigned after admitting to watching porn on his phone in the Commons.
The count was held in neighbouring Crediton because Tiverton school, the only facility in the constituency big enough to host it, was being used for exams.
As more and more ballot boxes rolled in, Lib Dem officials who started the night describing the race as "neck and neck" broke out into smiles.
At 2.22am party leader Sir Ed Davey effectively called the result. "Looks like I'm going to need a bigger hammer," he tweeted.
Looks like I'm going to need a bigger hammer 🟦🔨 👀
— Ed Davey MP 🔶 🇬🇧 🇪🇺 (@EdwardJDavey) June 24, 2022
The post referenced a photo op after last year's Chesham and Amersham by-election win which saw him knock down a blue wall of bricks.
An army of around 50 counters sifted through heaped up voting papers in a sports hall where the walls were cruelly painted in the sky blue of the Tory logo.
And it was the Conservatives who took a harsh beating as the count unfolded below posters advertising local taekwondo and kickboxing lessons.
Defeat piles more pressure on PM
The loss of Tiverton and Honiton will spark further unease amongst Tory MPs in the South West and beyond who fear losing their seats at the next election.
It also marks another stunning by-election victory for the Lib Dems, who have already overturned large majorities in North Shropshire and Chesham and Amersham.
There are only 40 constituencies in the entire country where the Conservatives have a bigger majority than they possessed in the rural Devon seat.
And there are 248 Tory MPs sitting on smaller leads over the Lib Dems, including Cabinet ministers like deputy PM Dominic Raab and Levelling Up Secretary Michael Gove.
Tiverton and Honiton voted to leave the EU by 58pc to 42pc, and the result will dampen suggestions the party can return to winning ways by returning to the Brexit battleground.
Mr Johnson was almost entirely absent during the campaign, making only one low-key visit during which he did not meet any voters, and he didn’t feature on local party leaflets.
Ahead of the contest the Prime Minister was already playing down expectations the Tories would hold onto the seat and dismissed questions he should resign as “crazy”.
"Governing parties generally do not win by-elections, particularly not in mid term. I’m very hopeful, but you know, there you go. That’s just the reality,” he said on Thursday.
Ms Hurford said in the run up to the vote that the fallout from partygate and the manner of Mr Parish’s resignation had made campaigning to hold the seat an uphill struggle.
Wakefield win hints at holes in Tory 'Red Wall'
In Wakefield, Labour's Simon Lightwood won a massive 13,166 votes to beat the Conservative candidate Nadeem Ahmed, who won 8,421 votes.
Mr Lightwood's victory signals potential Tory vulnerability in the 45 'Red Wall' constituencies that turned blue for the first time in a generation in 2019.
Labour will hope the victory is a sign that they can win back the loyalty of northern and working-class Britons who abandoned the party at the last general election.
The victory is also likely to lead to further questions over whether Boris Johnson will ever be able to regain public confidence following the partygate scandal.
Tory candidate Mr Ahmed backed Boris Johnson throughout partygate and said he remains a "great asset" to the Conservatives.
During his campaign, Mr Lightwood told voters: “Tomorrow, your vote could boot Boris Johnson out of Downing Street and deliver a fresh start for Wakefield.”
Wakefield had been a Labour seat since 1932 but the area voted Leave in the 2016 EU referendum, and the Tories overturned Labour's 2,176-majority in 2019 with their "Get Brexit done" campaign slogan.
Mr Lightwood, is a member of the party's national policy forum who works for the NHS.
He was chosen to represent Labour over trade unionist Kate Dearden by party members, but the entire executive committee of Wakefield’s local Labour group resigned in a row over the selection process.
They claimed Labour’s National Executive Committee intervened in the process and ensured all local candidates were “stripped out”.
Voters in West Yorkshire headed to the polls on Thursday following the departure of the city's previous Conservative MP, Imran Ahmad Khan.
In April, Imran Ahmad Khan - the MP for Wakefield from December 2019 until last month - was found guilty of sexually assaulting a 15-year-old boy.
On May 3, he officially quit his seat after his conviction. He was also expelled by the Conservative Party and has been jailed for 18 months.
In 2019, as part of Mr Johnson's 2019 general election landslide, Wakefield elected its first Conservative MP since George Hillman in 1931.
On that occasion Conservatives won 47.3 per cent of the vote, Labour 39.8 per cent, the Brexit Party 6.1 per cent and the Liberal Democrats 3.9 per cent.
On Thursday, sensing victory, a large number of prominent Labour politicians took to the streets in Wakefield to try and drum up some last minute support.
Shadow Health & Social Care Secretary Wes Streeting and Shadow Chancellor Rachel Reeves were among a group of around 10 MPs who spent the day knocking on doors and speaking to voters.