Liz Truss has been slammed for a "needless insult" directed at the French president, which has caused outrage across the Channel.
The Foreign Secretary, who looks likely to be the next PM, claimed the "jury is out" when asked if Emmanuel Macron was a friend or foe last night.
It drew loud applause from Tory party members at a hustings event in Norwich.
This morning Mr Macron responded by saying British and French people would always be friends despite mistakes by leaders - but warned that a lack of clarity could cause "serious problems".
And Chancellor Nadhim Zahawi tried to de-escalate the baffling row by claiming Ms Truss's comment was a joke which caused a lot of "chuckles".
Boris Johnson also intervened, describing Mr Macron as a "tres bon buddy" of the UK.
David Lammy, Labour's Shadow Foreign Secretary, voiced his disbelief at the astonishing remark about an ally while there is war in Europe.
He said: "At a time when the West must stay united in the face of Russian attempts to divide us, the fact the Foreign Secretary has chosen to needlessly insult one of our closest allies shows a terrible and worrying lack of judgement.
" Liz Truss ’ decision making has clearly become clouded by weeks and weeks of playing to the gallery of Tory members rather than focusing on the country."
Former Tory minister Gavin Barwell - who served as chief as staff under Theresa May, also questioned the remark, tweeting: "You would have thought the Foreign Secretary was aware we are in a military alliance with France."
Speaking to reporters in Algeria, Mr Macron said: “The United Kingdom is a friendly nation, regardless of its leaders, sometimes in spite of its leaders.”
He added: "Britain is a friend of France, I don't doubt that for a second... If France and Britain cannot say whether they are friends or enemies... then we are headed for serious problems."
Speaking to broadcasters during a visit to South West London Elective Orthopaedic Centre in Surrey, the Prime Minister was asked about Liz Truss's comments about the French president.
Mr Johnson said: "I think I've always had very good relations with Emmanuel Macron. Emmanuel Macron est un tres bon buddy de notre pays."
He added: "I think the relations between the UK and France are of huge importance. They have been very good for a long time, ever since the Napoleonic era basically, and I think we should celebrate that.
"As for Emmanuel, I've had very good relations with him and I can tell you something: he's a great, great fan of our country."
The German ambassador to the UK also warned that the relationship with France is of "crucial importance".
Miguel Berger, appearing on BBC Radio 4's Today programme, said: "I would say that the relationship with France is of crucial importance for the United Kingdom, so my recommendation would be really to look for a relationship that is as close as possible."
Pressed on whether Ms Truss's comments were wise, he said: "The relationship with France should be as close as possible.
"I think there needs to be an effort to reach a good understanding and cooperation with our French neighbours."
Mr Zahawi, defending Ms Truss, said she was trying to illustrate that British people judge others - even allies - by their actions and not their words, and said: "It was a light hearted comment and there were lots of chuckles around it."
"Stating the obvious, France is one of our closest strategic allies in defence and security, of course, in our effort to face down Putin in his illegal invasion of a free and democratic country in Ukraine," the Chancellor added.
"We like people to judge us on our actions, on our deeds, not words. And I think it is right that we also hold our allies to that very high standard."
Recent comments have suggested that a Truss government would have a frosty relationship with France.
Mr Macron reportedly described Boris Johnson as a "clown" as tensions escalated over Channel crossings.
In December he was claimed to have said: “It is sad to see a major country with which we could do huge numbers of things, led by a clown.”
It comes after Ms Truss distanced the UK from the prospect of a project of being part of a wider European political community following a meeting between Boris Johnson and the French president in June.
The Elysee Palace insisted that the Prime Minister had expressed interest in the idea, which would see non-EU states such as the UK involved.
Ms Truss denied the UK had ever been on board with such a proposal, saying afterwards: "That is not true.
"I don't know the exact words that President Macron has used, but we have not agreed to that."
Asked whether she bought into "his political and economic community", she replied: "No."
