Of these, 300,000 will be built within the existing urban boundaries and the other 100,000 on 5000ha to 6000ha of new land.
The 75:25 split is aimed at continuing with the former regional growth strategy to put the brakes on urban sprawl.
The plan is also built around a huge public transport programme that includes a $2.4 billion inner-city rail loop, rail to the airport and a new harbour crossing with rail to the North Shore.
But the emphasis on public transport worries the Government, which says it wants a more effective response to the expected growth in demand for travel.
"Careful decisions are needed to ensure that the future mix of projects provides sufficient new capacity to accommodate forecast growth" - a clear signal that the Government expects Mr Brown and the Auckland Council to put more emphasis on roads.
The Government has quoted figures in the draft plan showing vehicle traffic will remain dominant, vehicle trips will account for half of the growth in morning peak trips to 2041 and Aucklanders will make 5.5 million vehicle trips a day in 2041, an increase of 1.5 million trips over 2006.
Mr Brown's strong desire for tolls and congestion charges to help pay for the rail loop and other public transport projects also attracts a warning from the Government about the affordability and benefits to motorists - formalising concerns by Transport Minister Steven Joyce about the use of tolls to pay for public transport.
The 10-page response, from Local Government Minister Rodney Hide, challenges Mr Brown to do more work on the affordability, feasibility and phasing of his proposals, particularly those involving Government assistance.
"These processes will require considerable input and analysis before Government has sufficient confidence to make decisions on the allocation of funding resources for new investment," the document said.
On the compact city proposal, the Government has "reservations" about the plan to accommodate the predicted growth and what the trade-offs, such as apartment towers of up to 10 storeys in the suburbs, will mean for communities.
In a written statement, Mr Brown said that having set up the Super City to speak with one voice, the Government needed to listen with both ears.
Brown's plan:
* A $2.4 billion inner-city rail loop, rail to the airport and a new harbour crossing with rail to the North Shore, to be part-paid for through toll roads and congestion charges.
* The Government says: Aucklanders will make 5.5 million private vehicle trips a day in 2041, an increase of 1.5 million trips over 2006, and will be the main form of transport. The benefits of public transport must be balanced against the costs.