Electorates where the party vote turned from red to blue this election include former leaders Phil Goff and David Shearer's Mt Roskill and Mt Albert electorates.
National won the party vote in Mr Cunliffe's New Lynn electorate in 2011 but stretched that lead out further.
National Party pollster David Farrar noted Labour had not only come second in the party vote in most electorates, it was coming third in an increasing number as well, including Wellington Central.
In Auckland Central, Labour candidate Jacinda Ardern lost only narrowly to National's Nikki Kaye but Labour was well behind National in the party vote, just edging out the Greens for second place.
A Labour insider said the reason any party's candidate held their seat in spite of most voters favouring their opponents' parties was "personal brand".
"It's easier to protect a personal brand than it is to protect a party brand which you're only in very partial control of.
"In Labour's strongholds Labour's party vote is much more susceptible to nationwide trends than the electorate vote would be because people feel like they know their local MP - their local MP helped out someone on their street once or came to their community centre once in a way that the 'Labour Party' doesn't do."
Auckland University political communications specialist Jennifer Lees-Marshment said losing the party vote in electorates Labour held "shows a deep- seated dissatisfaction with what they're offering".
"If the voters are willing to vote for a Labour candidate but are not willing to vote for the party, that suggests that voters who are traditionally supporting Labour have concerns about the Labour Party.
"It means they've got a really big hill to climb to get the public's trust and respect back."
Political scientist Barry Gustafson said the way Labour had bled the party vote gave the impression "there's something wrong with their national campaign".
The party "has got to to watch that it isn't just seen as the party of Maori, Pacific Islanders and alternative lifestylers."
Click here for an interactive graphic showing every vote, seat and polling booth.