The Conservatives saw a majority of 24,000, or 40.6%, in the Devon seat of Tiverton and Honiton evaporate - a record reverse for the party - as the Liberal Democrats triumphed.

In Wakefield, the 'red wall' constituency in West Yorkshire snatched by the Conservatives in 2019, it was Labour that took victory.

Following the results of the by-elections, Mr Dowden resigned and said in a letter to the PM: "We cannot carry on with business as usual."

Mr Johnson thanked him for his service, but responded saying while he understood Mr Dowden's "disappointment", the government had a "historic mandate" from the general election and he wanted to continue working "to unite and level up" the country.

Chancellor Rishi Sunak also said he was "sad" at Mr Dowden's resignation, adding: "We all take responsibility for the results and I'm determined to continue working to tackle the cost of living."

Politics Hub: Reaction to Boris Johnson's humiliating defeats

It was the latest electoral mauling for the PM this year after the Tories lost nearly 500 council seats at the start of last month.

Simon Lightwood, who won the Wakefield by-election for Labour, said: "I think people are absolutely tired of the lies and deceit we've seen from the prime minister and they're demanding change and tonight is the demonstration of that."

Richard Foord, who took Tiverton and Honiton for the Lib Dems, used his acceptance speech to call for Mr Johnson "to go, and go now", claiming his victory had "sent a shockwave through British politics".

The prime minister has been under pressure over the partygate scandal as well as the cost of living crisis squeezing British household budgets.

That pressure intensified when a no confidence vote saw 148 Conservative MPs oppose him.

But in his damning letter, Mr Dowden upped the game again, saying: "Somebody must take responsibility."

Sir Roger Gale, a Tory backbencher and fierce critic of the PM, said Mr Dowden was "a decent and honourable man who has clearly decided that he can no longer defend the indefensible".

His Conservative colleague Angela Richardson - who resigned as a junior aide over partygate - also tweeted the former party chairman was "most certainly not responsible for these results", while fellow MP Simon Hoare said he was "proud to call Oliver a friend - never more so than today".

Mr Johnson, who is attending the Commonwealth Heads of Government conference in Rwanda, said ahead of the vote it would be "crazy" for him to resign as prime minister if he lost the two seats.

Sky News' political editor, Beth Rigby, said the exit of his chairman came as a surprise.

A source close to the PM said he took a brief phone call from Mr Dowden after he had made his decision public, which left him blindsided as the pair had been together on Wednesday to prepare for PMQs.

A Downing Street source admitted the resignation was not helpful and that they simply did not know whether more resignations would come.

But, given the vote of no confidence was held just weeks ago, the matter as far as the prime minister was concerned was settled.

Speaking after the results, Mr Johnson said he did not want to "minimise the importance" of the message from voters, but it was normal for governments to be "punished at the polls" in the middle of their term.

The PM added: "I think as a government I've got to listen to what people are saying, in particular to the difficulties people are facing over the cost of living, which I think for most people is the number one issue.

"We've got to recognise there is more we've got to do and we certainly will, we will keep going addressing the concerns of people until we get through this patch."

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But Labour leader Sir Keir Starmer said the Wakefield result showed the public "voting no confidence" in the government and it was time for the PM and his ministers to go.

Visiting the constituency to celebrate his party's victory, he added: "The Tory Party is absolutely imploding. They know they are out of ideas and out of touch.

"If they had any decency they'd get out the way for the next Labour government."

Speaking to Sky News, Liberal Democrat leader Sir Ed Davey said the South West by-election was a "huge victory" for his party, but also showed a "big issue for our country".

"I think the people of Tiverton and Honiton have spoken for the British people, and I think they have said loud and clear, Boris Johnson must go," he added.

"They do see him as a lying law-breaker and they see him as someone who doesn't have a plan for our country."

Analysis:
By-election losses will seep like poison slowly into the Tory bloodstream
Tories suffer some of the worst by-election defeats since 1945

The by-elections, both in leave-voting constituencies, took place on the sixth anniversary of the Brexit referendum.

They were each triggered by the resignations of Conservative MPs: in Tiverton and Honiton, Neil Parish quit after he admitted to watching pornography on his mobile phone in the Commons chamber; in Wakefield, Imran Ahmad Khan stepped down after being found guilty of sexually assaulting a 15-year-old boy.

Mr Parish told Sky News the Conservative defeat in his former constituency was down to "a combination of our vote dropping dramatically, people switching, people staying at home and a very unpopular prime minister which people have tactically voted against".

He added: "[Mr Johnson] has many good qualities. The trouble is he can't just keep living in a parallel universe - there has to be reality."

Wakefield's last Labour MP, Mary Creagh - who lost her seat to the Tories in 2019 - also said it was "very clear the public has fallen out of love with Boris Johnson".

Speaking to Sky News, she added: "All the rhetoric they were promised about 'levelling up' and 'the northern powerhouse' has been forgotten, and the Tory Party now looks like a project to keep one man in power."

Business minister Paul Scully said he was sad to see Mr Dowden resign, but he insisted to Sky News that the PM was still "the man for the job".

On the results, Mr Scully said: "It has not been a good evening by any stretch of the imagination.

"We have got to reflect, we have got to listen very carefully and we have got to respond. We need to prove to people we do have the answers."

But he said it was Mr Johnson's "brazen approach" that would come up with "the big ideas" to tackle the challenges facing the country, including the cost of living crisis.