After three weeks of campaigning around the country, Mr Cunliffe secured a resounding first-round leadership win on Sunday against fellow contenders Grant Robertson and Shane Jones.
But Mr Cunliffe's victory came through the strong support he received from the membership and affiliated trade unions.
Only 11 of his 34 caucus colleagues voted for him, a sign of lasting bitterness against the man in whom they now must put their faith to lead them to victory next year.
Prime Minister John Key has delayed his trip overseas to be in the debating chamber today to face Mr Cunliffe.
Mr Cunliffe, a superb debater and fast thinker who has a good grasp of policy, needs to make Mr Key sit up and take notice.
Mr Key was underestimated by former prime minister Helen Clark's minders during the 2008 election debates - to her cost.
Her predecessor, Phil Goff, was no match for Mr Key and neither was the latest leadership casualty, David Shearer.
Labour MPs realised the debating strengths of Mr Key, but did nothing to protect either Mr Goff or Mr Shearer.
Mr Cunliffe does not need the protection of his colleagues, but he does need their loyalty.
Labour has, since Miss Clark's resignation, been split asunder by in-fighting, personality clashes and trickery.
The Green Party has become the de facto Opposition, with co-leader Russel Norman often becoming the first stop for news media wanting a 30-second sound bite or hard-hitting quote. Reclaiming that role should come easily to Mr Cunliffe.
His speech on Sunday was peppered with the type of comments the party membership have been seeking.
Mr Cunliffe must lift Labour's support in the polls.
A honeymoon period is likely. Already one, albeit volatile, poll has Labour and the Greens well ahead of National and its coalition partner.
Labour needs the Green Party but, also, it needs to win back the support of the many hundreds of thousands of supporters who abandoned the party during the past two elections.
Being a strong performer in the House, against a formidable opponent such as Mr Key, is crucial for Mr Cunliffe's credibility.
While the debating chamber is dismissed by many as irrelevant to the actual leadership of a party, being seen as strong or weak by commentators plays a tremendously important part in the perception laid out across all forms of media - traditional to social.
Mr Cunliffe also needs to make some changes to the Labour line-up.
His selections for key positions will help or hinder his chances of competing with Mr Key at the next election. In a presidential-style campaign, Mr Cunliffe will thrive - but, again, the support of his colleagues is crucial.
That said, he is unlikely to fall for some of the tactics exercised against Mr Shearer which played up his ineffectiveness.
The same people who worked against Mr Shearer will find Mr Cunliffe made of sterner stuff.
Mr Cunliffe needs to put into positions of influence people he can trust, and he needs to do it soon.
Labour was leaderless for three weeks, and still went up in the polls.
Some Labour MPs were scathing about Mr Cunliffe when he was beaten in the contest won by Mr Shearer.
They should expect to be shown the door.
Mr Cunliffe has fewer MPs to work with, but the talented ones are obvious.
They need promoting, on the proviso that one murmur or hint of disloyalty will see them out.
Mr Cunliffe has the support of the rank and file, who took it upon themselves to punish the caucus for electing Mr Shearer instead of Mr Cunliffe in 2011.
He needs to take confidence in that result and build around him a team he can trust.
Most of his colleagues did not want Mr Cunliffe as leader, but strong performance should bring them around.
Mr Cunliffe has offered to run a meritocracy, where people are promoted on ability.
But a leader needs to lead, and being Opposition leader must be seen as an audition for the job as prime minister.
After successfully winning one job, the casting call for the top job begins today.