Also known as H2A, Hei Awarua ki te Oranga stretches from Papakura in the north to Cambridge and Te Awamutu in the south.
Urban Development and Transport Minister Phil Twyford said it was the first time two regions in New Zealand had joined together with the Government to implement such a plan.
"Waikato-Tainui and the local councils are well used to working together and I'm pleased central government is now to join them on this important project for both regions' future."
Maori Development and Associate Housing Minister Nanaia Mahuta said the partnership aimed to unlock the "significant growth potential in Southern Auckland and the Hamilton-Waikato metropolitan area, underpinned by new rapid and commuter rail connections".
"The transport network will direct where much-needed housing will be developed and connect our people to growing employment opportunities in both the Waikato and Auckland."
Hamilton would be poised to become an "even higher growth but affordable urban centre", she said.
"Strategic planning will protect and enhance the quality of both regions' natural environments, as well as their cultural heritage.
"It will boost supply of affordable housing options to the communities that need them most."
At the core of the corridor are the Waikato and Waipa Rivers, the Main Trunk Line and the Waikato Expressway.
Twyford said the initiatives could strengthen connections including walking and cycling trails along the Waikato River to Manukau Harbour, new intercity rapid rail services and a new mass transit network for the emerging Hamilton-Waikato metropolitan area.