Jean-Marc Ayrault, who called Mr Johnson a liar last week over his claims during the EU referendum, said he did not take the Hitler remarks personally.
The French Foreign Minister said: "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, who discusses it reasonably, 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 Johnson caused widespread anger during the Brexit campaign when he compared the ambitions of the EU with those of Hitler.
Dutch foreign minister Bert Koenders said everyone was waiting to see if Mr Johnson still had the same views on the EU.
The spat came as Mr Johnson insisted the EU could remain a "docking station" for the UK after Brexit.
The former Vote Leave frontman said: "The point I was making there is that we are very keen to see the EU develop and go forward and all we would say is that there are kind of docking stations and doorways open for further UK involvement down the track."
But in a sign of the tough negotiations ahead, Brussels warned that EU nationals in the UK must be treated with "dignity" as the UK Government continues to refuse to guarantee their status.
By Matt Payton