Those gathered applauded as Ardern said local people would have first priority for the KiwiBuild homes.
She also announced 150 new state houses in other parts of Porirua.
"The scale and ambition of what we're intending might happen once in a generation," she said.
"The Wellington region has not seen a project of this scale and ambition since the time that Porirua City was first built.
"This is a huge, long-term, generational investment."
She reassured current users of social housing that their rights would remain the same and their rents would not rise as a result of the revitalisation.
Local MP Kris Faafoi said Porirua East had a "proud history".
After the war a "huge project" was set about to create more housing in the city, he said.
"People moved to Porirua to make a new life, many from different cultures, which has made our community richer."
Ngāti Toa Rangatira chief executive Tā Matiu Rei said the iwi supports the concept of a "reset" for Porirua.
He welcomed the opportunity for Ngāti Toa to manage 900 of the public housing properties.
"This is an extremely important step for us as an iwi [and] as an integrated provider of health services ... housing is an important determinant of wellbeing and health."
Ngāti Toa runs five health centres around the Wellington region.
Mayor Tana said today was "indeed a great day".
"This is the biggest thing that has happened in the Wellington region for so long.
"Our families can look forward to having warm, dry, affordable houses."
The project would also provide employment opportunities for locals and would boost the business sector, he said.
"Porirua is poised and ready for this sea change moment.
"This is about Porirua, this is about our city, but this is also about our country. This Government has made a commitment to serve the wellbeing of our people."
Pointing to Ardern's speech to the United Nations General Assembly in September, Tana today was "all about kindness".
