Suella Braverman has been accused of "sowing the seeds of hatred" by Sir Keir Starmer after her comments about the police and pro-Palestinian marches.
The Labour leader took aim at the home secretary after she branded pro-Palestinian demonstrations, including one which took place on Saturday in central London, "hate marches" and accused the police of "double standards" in the way they handle protests.
Sir Keir said few people in public life had "done more recently to whip up division, set the British people against one another and sow the seeds of hatred and distrust than Suella Braverman".
Follow live: Tension remains on London streets
"In doing so, she demeans her office," he wrote in the Sunday Telegraph.
Bringing the prime minister into view, Sir Keir said Ms Braverman and Rishi Sunak's treatment of the police and protesters showed a "lack of respect for this country's values and its principles" after the pair urged police to ban the Armistice Day demonstration.
It follows calls from numerous senior political figures for Ms Braverman to resign, after they blamed her for violence that broke out in the capital.
On Saturday, a total of 126 people were arrested in London.
This included 92 people who were arrested in Pimlico, central London. The Metropolitan Police said they were part of a large group of counter-protesters who tried to reach the main pro-Palestinian march in the capital.
Police later said the arrests included a number of pro-Palestine protesters who were detained after a group broke away from the main demonstration.
The demonstrators were wearing face coverings and firing fireworks, some of which struck police officers in the face, Assistant Commissioner Matt Twist said.
Mayor of London Sadiq Khan said the scenes of disorder were a "direct result of the home secretary's words", adding that the police's job had been made much harder as a consequence.
While shadow home secretary Yvette Cooper called for "calm", with a swipe at Mrs Braverman for fuelling tensions.
"Everyone must reflect on the impact of their words and actions. It is the responsibility of all of us to bring people together over this weekend, not divide and inflame," she posted on social media.
Former Labour leader Jeremy Corbyn was one of those in attendance at the march.
Addressing crowds from on top of a fire engine near Vauxhall, he said Mr Sunak and Ms Braverman's attempt to stop the march from going ahead has been "shamed".
"It seems that there's one million of us here today in London showing our solidarity with the people of Palestine, so Suella Braverman and Rishi Sunak's attempt to stop this has been shamed for what it is," he said.
"They should be ashamed also (of) their vote on the United Nations when they wouldn't even support a call for a ceasefire in Gaza. Shame on them."
Ms Braverman asserted that she had given police her "full backing" at a meeting with Metropolitan Police Commissioner Sir Mark Rowley on the eve of Armistice Day.
He wrote: "The far right has been emboldened by the home secretary. She has spent her week fanning the flames of division. They are now attacking the police on Armistice Day.
"The home secretary's position is untenable. She must resign."
Nine officers were injured as they prevented a crowd of mainly "football hooligans" reaching the Cenotaph, with Mr Twist calling their "extreme violence" towards the police "extraordinary and deeply concerning".
Officers later clashed with protesters from both sides in Chinatown and Victoria station.
Mr Twist said "a week of intense debate about protest and policing" helped "increase community tensions".
'Rishi Sunak is responsible'
On Friday, Mr Sunak maintained "full confidence" in his home secretary, even after some ministers had already distanced themselves from her after she claimed some people were homeless as a "lifestyle choice".
He defied calls from Labour and the Liberal Democrats to sack Ms Braverman, but there has been speculation that a ministerial reshuffle could see the home secretary moved.
Layla Moran, a Liberal Democrat MP who has family in Gaza, said the blame for any trouble caused by far-right groups lay with Mr Sunak.
"As the police in central London work to contain the far-right, and everyone starts to blame Suella Braverman, just remember who chose to not only give her the job but also chose not to sack her," she wrote on Saturday.
"Rishi Sunak is as, if not more, responsible for what happens today".
Defence Secretary Grant Shapps, Shadow home secretary Yvette Cooper and SNP Westminster leader Stephen Flynn are appearing on Sunday Morning with Trevor Phillips from 8.30am today.