Andy Burnham said Labour must stop the 'politics of poison seeping into our streets' after scenes of unrest at anti-migrant protests over the weekend.
Speaking to MPs and peers at a closed-doors meeting on Monday, the Prime Minister said the party's mission must be to counter 'fear with positivity and hope'.
It comes after crowds of masked men blocked road access to the Port of Dover on Saturday and official vehicles were damaged with a handful of police officers injured during a stand-off with protesters in Portsmouth on Sunday.
Mr Burnham is understood to have told the Parliamentary Labour Party (PLP) that Britain would never accept any form of racism in its communities and stood for a sense of fairness and justice.
'We've got a fantastic opportunity in our hands to change this country for the better. We go into the autumn, in really good heart, with a spring in our step,' the Prime Minister said.
'There's a lot at stake and it requires us to counter fear with positivity and hope. We have a responsibility in the times that we're living in. It's a solemn responsibility to prevent the politics of poison seeping into our streets.
'We are here to speak to the politics of hope and of positivity.'
Setting the tone ahead of party conference in the autumn, the Prime Minister said his government would be 'boldly, authentically, confidently Labour' and focus on making the public believe that politics can work.
'We have to fulfil our historic mission all over again and bring hope to a divided country. To lift people and make them feel that things are possible. That we can make people's lives better,' he said.
'Never accept the narrative that there's nothing we can do.'
More than 200 protesters attempted to stop coaches which were due to take migrants for processing after around 120 people arrived in a boat near the Isle of Wight in the early afternoon on Sunday.
Policing minister Sarah Jones warned earlier there was 'no excuse' for threatening behaviour or serious disruption and any demonstrators who crossed the line from peaceful protest into illegality would 'face the full force of the law'.
She told the Commons that Patriot Platform, the group which claims to have organised the protest in Dover, was 'far-right racist'.
Responding, shadow home secretary Chris Philp said the right to protest 'should never be violently exercised', but criticised the Government's record on migration.
'If they're serious about fixing this and ending public anger, they need to get serious about the measures – leave the ECHR (European Convention on Human Rights) and deport illegal immigrants as soon as they arrive.
'Then people won't be so angry,' he said.
The demonstration at Dover appeared to have come as a surprise to the authorities, with Kent Police claiming it was 'spontaneous'.
Hampshire and Isle of Wight Constabulary has launched an investigation into potential assaults and criminal damage following the unrest in Portsmouth.
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