Auckland, Christchurch, Dunedin, Rotorua and Nelson have all elected centre-right mayors in polls marked by low turnout and dissatisfaction with a key policy of Ms Ardern's government: Three Waters.
Those cities alone account for roughly half of New Zealand, marking a sharp shift from previous governance.
In Whanganui, even Ms Ardern's own cousin Hamish McDouall lost out after two terms in charge.
There are good reasons to be skeptical that local government results can predict a central government election, due late next year.
The National party does not run candidates, and Labour only endorsed a handful across the country, with varying levels of support from HQ.
"I've never been one to read particularly into local government elections," Ms Ardern told Radio NZ.
"You see it move in its own rhythms across the country ... 37 mayors have just been re-elected as well."
Still, the result in Auckland - home to 1.7 million people or a third of Kiwis - has the potential to cause Ms Ardern and Labour plenty of grief.
Cantankerous septuagenarian Wayne Brow became the first right-leaning Auckland mayor in 12 years, crushing Labour's endorsed candidate Efeso Collins with 144,619 votes to 89,811 - a margin which surprised many.
Showing his unorthodox streak, after winning Mr Brown cancelled planned media, ordered a full briefing on the council's spending, went surfing and took a helicopter ride to "survey the realm" as he told the NZ Herald.
Mr Brown was one of many to campaign against Three Waters, Labour's multi-billion dollar plan to fix ailing drinking water, storm water and waste water systems across New Zealand, which strips councils of control of that infrastructure.
"There is real anger around the government on Three Waters," successful Nelson candidate Nick Smith told TVNZ.
"Unless the government has a death wish, they do need to revisit that."
Speaking on Monday morning, Ms Ardern suggested some appetite to do so.
"The alternative to Three Waters is rate rises in the $1000s because of the additional water infrastructure that is required, no one's out campaigning on that," she said.
"We've been open to making changes to try and make these the most effective changes that we can."
Alongside Mr Collins, Ms Ardern personally endorsed just one other candidate, her own MP Paul Eagle, who stood in Wellington, New Zealand's most left-wing city.
He came fourth in an embarrassing result for the Rongotai MP and the party, which lost out to Green candidate Tory Whanau.
In Dunedin, outgoing Green mayor Aaron Hawkins said he saw a clear appetite for change across New Zealand.
"We're seeing around the country we're experiencing a push against the establishment, whatever that looks like, and we are not immune to that," he told Radio NZ.
Ms Ardern was one of many to express dismay with turnout, which sat below 40 per cent nationwide and lower still in poorer areas.
"What is absolutely clear in my mind is we can't just stick with the status quo," she said, suggesting support for a shift from postal to in-person voting.
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