Jean-Marc Ayrault, who branded Mr Johnson a liar last week over his referendum claims, said he did not take the Hitler remarks personally.
“No. He did not apologise. I did not feel it targeted me when he said that, nobody around the table did.
“Everyone knows what the EU is. Everyone knows, that the EU presents a great opportunity for freedom, democracy and for prosperity.
“So Boris Johnson, I would say, came to this council with some humility,” Mr Ayrault said.
EU foreign affairs chief Federica Mogherini sidestepped the question when asked if the Hitler comments would make yesterday’s gathering, which included talks with US secretary of state John Kerry, “awkward”.
Mr Johnson caused widespread anger when he compared the ambitions of the EU with those of Hitler, in the Brexit campaign.
Dutch foreign minister Bert Koenders said everyone was waiting to see if Mr Johnson still had the same views on Hitler.
Mr Kerry insisted the EU was a force for good as he pointed out that America and Europe together had defeated fascism.
The Hitler spat came as Brussels warned that EU nationals in the UK must be treated with dignity as the government continues to refuse to guarantee their status.
With Brexit Minister David Davis floating the idea of a pre-withdrawal cut-off point, after which migrants will not be allowed full rights, the EU called for “calm”.
Commission president Jean-Claude Juncker’s spokesman said concerns around the 1.2 million Britons living in the EU and the three million EU nationals in the UK could only be sorted out once the UK triggered formal exit negotiations.
“In the meantime I think that when dealing with these issues we have a common interest to appeal for calm and dignity.
“We are talking about people now, so all sorts of statements and acts should be firmly anchored in the law,” he said.
The spokesman emphasised that all citizens across the Brexit divide retained their full rights for as long as the UK remained a member of the EU.
Mr Johnson used his debut on the world stage to insist Britain would not “abandon” its leading role in Europe.
Mr Kerry welcomed the remarks, saying: “Boris Johnson made clear today in his own comments that the United Kingdom intends to remain a critical, vital, strong component of the European relationship, and of the United States’ relationship with Europe.”
Meanwhile, Mr Johnson has quit his lucrative newspaper column, and a commission to write a book on Shakespeare has been put on hold.
He has ended his £250,000 contract to write a weekly article for the Daily Telegraph following his appointment to the Cabinet.
Hodder & Stoughton has postponed publication of Shakespeare: The Riddle of Genius – which had been due out in October, but it expects to release the work in the future.
Mr Johnson received an advance of around £90,000 for the book.
Mr Johnson’s outside earnings from writing saw him pay nearly £1 million in tax in four years, documents he released earlier this year showed. Over four years, he was paid £987,097 for his Telegraph column – while book royalties brought in a further £469,385.