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The First Minister was left badly wounded after a historic SNP defeat in Aberdeen South saw the Tories surge from third place to win with 50 per cent of the vote.
Douglas Lumsden’s ‘stunning’ victory was the first Westminster by-election gain in Scotland for the Conservatives since 1967.
Economy Secretary Stephen Flynn, seen as Mr Swinney’s likely successor, immediately took a coded swipe at his boss for the loss of his old seat.
He said some in the party needed to reflect ‘quite heavily’ on a ‘tough night’, triggering a bout of infighting among the Nationalists.
Mr Swinney’s standing then took a further battering just hours later after a damning court ruling rejected his plan to cage biological males in women’s prisons.
One former SNP cabinet minister said it was ‘only a matter of time before Flynn forces Swinney out of the top job’.
It comes as Sir Keir insisted he would carry on despite Manchester mayor Andy Burnham winning the Makerfield by-election. Mr Burnham made clear he plans to take over as prime minister and try to reviltilise Labour on his return to Westminster.
John Swinney is under pressure after the SNP lost Aberdeen South
Speaking after his victory, he said: ‘It is our last chance to change, but we’re going to take it.’ The PM reportedly called ministers to explain his wish to carry on and avoid the ‘chaos’ of a leadership contest.
Mr Burnham is expected in London on Monday to meet Labour MPs in readiness for a move against Sir Keir if he refuses to budge after a weekend’s reflection.
Scottish Tory leader Russell Findlay said: ‘While Andy Burnham has Keir Starmer firmly in his sights, Stephen Flynn’s desire to swipe John Swinney’s job is an open secret.
'Following my party’s by-election victory, both of these lame duck leaders must wake up to the critical importance of our world leading oil and gas industry.
‘The tragedy is that thousands of Scottish jobs are being lost while these two gigantic egos are only interested in their own jobs.’
The Aberdeen South result was a humiliation for Mr Swinney and the SNP.
It was the First Minister’s first electoral test since the SNP former chief executive Peter Murrell pleaded guilty to embezzling £400,000 from party funds.
The successful Tory strategy was to turn the contest into a local referendum on the future of the North Sea.
Mr Lumsden and Kemi Badenoch highlighted the SNP’s weak support for the industry, its ‘presumption against’ new drilling and ties to the fossil fuel-hating Scottish Greens.
They said only the Conservatives will stand up for the industry.
The result was Labour, Liberal Democrat and some former SNP voters voting tactically for the Conservatives.
SNP candidate Richard Thomson saw his party’s 2024 majority of 3,758 vanish and replaced by a lead of 6,050 for Mr Lumsden as the Tory vote share doubled.
Reform UK’s Jo Hart was third, while Labour’s Nurul Hoque Ali was fourth.
Turnout was 38.1 per cent, down from 59.9 per cent at the last general election.
Mr Flynn, one of the SNP’s most vocal supporters of the oil and gas industry, writing on X , said: ‘A tough night in Aberdeen that some will need to reflect on, quite heavily.
‘Commiserations to my good friend Richard Thomson - a great man and colleague.
‘Congratulations to Douglas Lumsden. I know he loves this city as much as I do, and I look forward to working with him.
‘We lost Aberdeen South to the Tories in 2017, and we won it back two years later.
‘I’ve no doubt that we can do so again. If we get things right.’
The comments, written as Mr Flynn attended the World Cup in America, prompted a backlash from one of Mr Swinney’s closest allies.
Former special adviser Kate Higgins reminded Mr Flynn, whose move to Holyrood last month was partly driven by his ambition to become First Minister, had triggered the by-election.
She wrote: ‘I do hope that “some” includes you Stephen Flynn - the by-election was, after all, caused by your choices.’
The infighting led to speculation that Mr Flynn was ‘on manoeuvres’.
Former SNP health secretary Alex Neil said: ‘It’s only a matter of time before Flynn forces Swinney out of the top job.’
Sir Keir Starmer is facing a prospective leadership challenge from Andy Burnham
Another SNP source said: ‘The fudge on oil and gas showed Swinney’s inability to break free of the Sturgeon era.
‘Stephen Flynn will always be on manoeuvres - he should be. John Swinney cannot read a room.’
Mr Swinney said the Tories had tapped the ‘understandable anger’ felt by voters seeing the oil and gas sector lose 1,000 jobs a month.
He added: ‘In Aberdeen South, the Conservatives were able to mobilise a very strong tactical voting campaign and also a campaign that captured the anger and the frustration of people in the north-east of Scotland and in Aberdeen, especially in relation to oil and gas.
‘I have to acknowledge that and I have got to consider the implications of that for the SNP and the government.’
Asked if Mr Flynn was right to say there should be more reflection on messaging, Mr Swinney said: ‘I think we have all got to do that.’
Although the SNP has no power over energy policy or licensing, its attitude and preference for funding renewable projects is seen as critical to would-be investors in the North Sea.
Despite the crushing loss in Aberdeen South, the SNP comfortably held on in the other Scottish by-election on Thursday, improving their majority in Arbroath and Broughty Ferry.
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