It is expected that 50,000 fans will pack the stadium for the Queensland versus New South Wales match.
Auckland Mayor Wayne Brown said securing State of Origin reflected the city's strength as a major sporting centre.
"From the outset, Auckland made it clear we wanted to bring State of Origin to our city, and we've worked hard to secure it," he said in a statement.
"We know how to host major events, and we know the value they bring. This match will mean full hotels, busy restaurants and bars, and thousands of visitors experiencing everything our region has to offer."
Hosting State of Origin is expected to attract more than 10,000 international visitors from Australia, generate nore than 50,000 international visitor nights, and inject an estimated $17.4 million into the Auckland economy.
Australian Rugby League Commission chairman Peter V'landys said the historic clash would give New Zealanders the opportunity to experience the intensity of the game's greatest rivalry.
"Rugby league is the No 1 sport in Australia and the Pacific, and the growth we have seen in New Zealand over recent years has been nothing short of extraordinary," V'landys said.
Sir Graham Lowe, the only New Zealander to coach a State of Origin team as a former Queensland coach, said the occasion would be one to remember.
"Kiwis are excited about State of Origin, but there are only a few of them that have had the opportunity to actually watch it live. This will be a fantastic occasion for Auckland," he said in a statement.
The 2027 fixture is being co-funded in partnership by Auckland Council Events and the New Zealand Government via the Major Events Fund.
