This led to accusations of undermining the Australian Government.
Ardern, who had just taken over the party leadership at the time, called Hipkins' actions wrong, but took him at his word that he did not know the questions were about Joyce.
This afternoon Ardern repeated to the Herald that Hipkins' actions were inappropriate.
"We were not directly aware of Mr Joyce's situation at the time that Chris asked the questions he did, and maintain that, of course, he should never have asked them.
"But this was not something we were directly involved in."
Asked if she had any sympathy for Joyce she said: "I've certainly observed situations like this where politicians have been caught off guard through no fault of their own.
"I've seen it happen here in New Zealand before," she said, referencing former Labour MP Harry Duynhoven, who put his seat in jeopardy when he applied to resume his citizenship of the Netherlands. He had lost his Dutch citizenship due to a law change there, and did not know that applying for foreign citizenship would have required him to vacate his New Zealand seat - but the New Zealand Government amended the law.
Contacted by the Herald about the High Court judgement, Hipkins declined to comment.
A byelection in Joyce's New England where he will attempt to regain his place will become a major political showdown with Labor hoping to harm the entire Government.
Joyce and Senators Fiona Nash, Malcolm Roberts and Larissa Waters and Scott Ludlam were also disqualified.
Senator Nick Xenophon and Matt Canavan were the only two out of the "citizenship seven" not to be struck out.
Insiders have today been abuzz over the speculation of the future of the senators, in particular Joyce.
If kicked, it could cause a huge headache for Malcolm Turnbull's one-seat majority government.
The politicians, dubbed the "citizenship seven" were referred to the High Court after Greens senator Scott Ludlam resigned in August over his dual citizenship status with New Zealand. In Australia, the constitution bans politicians from sitting in parliament if they hold citizenship to another country.
But no one - even some of Canberra's most seasoned insiders - was confident which way the High Court would swing its gavel.
In Canberra, Prime Minister Turnbull's focus was on the future worst case scenario, in case of Joyce's disqualification.
With Turnbull scheduled to leave for Israel this weekend, the question of whether the Deputy Leader Joyce would step in during his absence was high on the PMO's agenda.
If Joyce was disqualified, Deputy Liberal Leader and Foreign Minister Julie Bishop was a candidate to step into the role but Nigel Scullion, the Deputy Nationals Leader, was also an option.
Or, with his government in crisis, Turnbull might have to cancel his trip.
But with Joyce seen furiously signing ministerial documents in the last sitting of Question Time, onlookers saw it as a sign he was confident of a win, or "trying to get his ducks in a row".
The government argued Joyce and four others were unaware they had inherited citizenship of another country and took steps to renounce it as soon as they realised.
The two excluded from the government's fight were Greens Senator Scott Ludlam and One Nation's Malcolm Roberts.
Ludlam was born in New Zealand, while India-born Roberts had failed to renounce his UK citizenship, the High Court found in September.
Senators Matt Canavan, Fiona Nash and Joyce were born in Australia but were citizens by descent.
"The constitution as everybody understood it up until now was that if you had foreign citizenship, well that was it: you were out," Constitutional law expert Professor Anne Twomey told Sky News.
"The obligation is on you to sort it out. There's still a very strong argument that at least on the basis of the law as we knew it...people should have done due dilligence, and he (Barnaby Joyce) didn't."
