“Tempers need to come down, and people need to come together because it’s only by getting Brexit done that you’ll lance the boil of the current anxiety and we will be able to get on with the domestic agenda,” he said on Thursday.
Mr Johnson faced fierce backlash after he dismissed a complaint by one Labour MP that his “inflammatory” rhetoric risked provoking attacks on parliamentarians as “humbug”.
He has refused to apologise for those comments.
Despite this, the PM admitted he would need cross-party support for any new deal negotiated with the EU.
“I need to reach out across the House of Commons,” he said.
“I think it is fair enough to call the ‘surrender act’ what it is. I think it is absolutely reasonable. But we do need to bring people together, and get this thing done."
However, former Tory Prime Minister John Major has accused Mr Johnson of “wilfully” destroying the prospects of cross-agreement on Brexit after the language row, and turning the Tory party into a “Brexit party tribute band”.
“Most Conservatives are not a Brexit Party tribute band, nor have we abandoned our core values to find compromise, seek allies, and strive for unity, rather than division and disarray,” he said in a speech for the Centre for European Reform.
“We abhor the language of division and hate – and words such as ‘saboteur’, ‘traitor’, ‘enemy’,‘surrender’, ‘betrayal’ have no place in our party, our politics, nor in our society.
“It is emphatically not who we are as a people. And must never be seen as so.”
The former conservative leader also described Mr Johnson’s tactics of whipping up “fear and anger” as “profoundly unconservative”.
Sir John added that Mr Johnson had only paid “lip service” to the Supreme Court ruling and warned he could the PM should bypass the law designed to prevent him forcing the UK out of the EU without a deal – otherwise known as the Benn Act.
Opposition leaders met on Thursday night in cross-party talks to prevent the PM from doing so.
Jeremy Corbyn held cross-party talks in his Westminster office on Thursday over fears the Prime Minister will refuse to ask the EU for an extension as required by the Benn Act.
The Labour leader spoke with the SNP’s Westminster leader Ian Blackford, the Liberal Democrats’ head Jo Swinson, the Independent Group for Change’s Anna Soubry and Plaid Cymru’s Liz Saville-Roberts.
The discussion focused on how to prevent the PM ignoring the Act, which opposition MPs and Tory rebels passed to demand him to ask for a delay to Brexit until January 31, unless they back a deal.
Mr Corbyn, in an interview after the meeting, said they will take “parliamentary action” to ensure the PM does not “crash us out” of the EU on the current October 31 deadline without a deal.
“It’s not a matter of choice for him, it’s an Act of Parliament that was passed. Last night he seemed unable to give that undertaking,” Mr Corbyn said.
The leaders are set to meet again on Monday to discuss what motions they can introduce in the Commons to further force the PM to request the delay from Brussels.
They also condemned Mr Johnson’s rhetoric on Brexit, in light of Ms Swinson having left the meeting early to speak to police about a threat made against one of her young children.
Mr Corbyn alleged that the PM was encouraging people to act in “disgraceful and abusive” ways.
Meanwhile in the Commons, Mr Johnson has been heavily criticised by MPs for sending a junior government minister to answer questions about controversial remarks made in the House of Commons.
The prime minister came under fire for calling a law aimed at blocking a no-deal Brexit the "surrender bill", and for claiming that murdered MP Jo Cox would have wanted to get "Brexit done".
Labour MP Jess Phillips revealed that a man had been arrested on suspicion of trying to smash the windows and kick the door of her Birmingham Yardley constituency office.
While she said she would not “leap to blame” Mr Johnson for the specific incident – which saw staff lock themselves in for their own safety – she accused him of pursuing a “specific strategy” to provoke hatred.
“What he is doing is not human. It is manipulative, it is purposeful, it is his strategy. He wants people like me to be under threat,” she said.
Her comments were echoed by Paula Sherriff, the Labour MP who remonstrated with the Prime Minister, in the Commons chamber.
“I believe the Prime Minister is inciting hatred towards MPs,” she said.
Mr Johnson insisted he deplored any attacks on MPs – particularly women, but defended his actions and his comments in the house.
“I totally deplore any threats to anybody, particularly female MPs, and a lot of work is being done to stop that and give people the security that they need,” he told BBC North West.
“But I do think in the House of Commons it is important I should be able to talk about the surrender bill, the surrender act, in the way that I did.”
Commons Speaker John Bercow pleaded with parliamentarians on all sides to tackle the “toxic” political culture, and said the House “did itself no credit” in the angry exchanges which followed the Prime Minister’s statement.
As MPs returned to the Commons on Thursday morning, Mr Bercow said: “There was an atmosphere in the chamber worse than any I’ve known in my 22 years in the House.
“On both sides passions were inflamed, angry words uttered, the culture was toxic.”
Even the Prime Minister’s sister, Rachel Johnson, hit out at her brother’s “strongman” tactics, accusing him of using the Commons despatch box as a “bully pulpit”.
“What we are seeing is an executive that is so keen to deliver Brexit in any shape or form … they will do anything to justify that end,” she said.
The PM's often-silent senior adviser Dominic Cummings has come out to defend his boss' comments.
When asked if he blamed MPs for the abuse they were getting at a book launch on Thursday, Mr Cummings said: "The MPs said we will have a referendum, we will respect the result and then they spent three years swerving all over the shop.
“People on all sides have said things that veered between unwise and very unpleasant, and sometimes criminal.
"That is true of people of the Leave side and that's true of people on the Remain side.
He added: "People have been running around during the referendum campaign saying I was a Nazi, they run around for three years afterwards saying I am a criminal, and now a criminal Nazi."
At Westminister, Mr Cummings was filmed being confronted by Labour MP Karl Turner, after he had received death threats from his constituents overnight.
In the video, the PM’s advisor could be heard responding with: “Get Brexit done.”
Nigel Farage, leader of the Brexit Party, told a rally conference in Maidstone that he doesn't regret using words such as 'surrender' and 'betray' during the Brexit campaign either.
He said: "What I've seen their trolling, what I've seen their physical violence now have the temerity that we shouldn't use words like 'surrender' and 'betray'.
Farage also thanked Tory grandee Ken Clarke for saying that Boris Johnson's use of language of the Brexit vote being betrayed came from him.
Feelings were running high following the Supreme Court ruling that Mr Johnson’s five-week prorogation of Parliament had been unlawful.
However, he risked provoking further anger after it was suggested that he could skip Prime Minister’s Questions next week in order to deliver his set piece party conference speech.
MPs voted to reject a Government motion for a three-day break, while a Tory conference is taking place in Manchester, intended to allow MPs and ministers to attend as normal.
However a Tory source insisted the event would go ahead anyway, adding: “If somebody needs to do PMQs, somebody will do PMQs.”