Te Papa chief executive Courtney Johnston said charging an entry fee was necessary to fund the rising energy, insurance and staffing costs for the museum.
She said it was only partly funded by the government and needed to earn an additional $30 million per year.
"Te Papa is free for all New Zealanders - and it will stay that way," she said.
"Charging international visitors will help fund the incredible experience for everyone who walks through our doors.
"This is a considered and necessary decision to ensure that Te Papa can continue delivering a world-class experience in the face of rising costs."
The entry fee will be $35 and will apply from 17 September to international visitors aged 16 years and older.
With nearly 600,000 international visitors in the 2023/2024 financial year, Te Papa is expected to earn an additional $20 million per year from the move.
The remaining $10m needed will come from commercial activities - cafes, retail stores and car parking - and donations.
Johnston said visitors would self-identify their nationality.
"You'll walk into Te Papa and we'll say, 'Kia ora, how are you? Where have you come from today?' And if you say, 'Oh, I've come from Johnsonville', then we'll say, 'Great, head up the stairs, head into the museum, have a wonderful visit'.
"And if you say, 'Oh, I'm from France' or 'I'm from Germany', we'll say, 'Awesome, head up the stairs, you'll see the ticket desk right there, that's where you can buy your ticket'."
