The plans, part of a 30-year scheme to reshape the town, cover more than 50 ha at densities of up to three times the national average.
A spokesperson for English Partnerships said: "There is a feeling that Milton Keynes is hugely underdeveloped and used mainly as a shopping destination.
"The centre needs a vibrant urban feel to it with people actually living here."
Proposals for the Sustainable Residential Quarter, drawn up by Rick Mather Architects, include 2400 rented, affordable and key-worker homes, communal gardens and a school.
Plans for Campbell Park, prepared by EDAW, include 1800 homes, a marina with mooring facilities, restaurants and a bridge connecting the development to the town centre.
Executive director of English Partnerships Dennis Hone said: "We want to create two new sustainable central communities that offer increased housing choice within Milton Keynes, supported by a wide range of local facilities."
Masterplans for both areas will be drawn up later this year, with work expected to begin on the first phase in 12 months' time.