The moves come as housing provider Kainga Ora attempts to divest large swathes of its land in response to a government review that said its debt was "unsustainable".
Among the land listed online is Albertson Ave, which was originally going to provide 12 properties in Port Chalmers.
Real estate firm Colliers has been tasked with the sale of the land. The sale deadline is October 7.
"Nestled in the picturesque locale of Port Chalmers, just 15 minutes from the Dunedin CBD but offering a quiet suburban life, this site awaits a proactive developer or investor to take it forward and to take advantage of the lack of level-contour development sites in the wider Dunedin market," the listing said.
West Harbour Community Board member Duncan Eddy said the announcement was a "disgrace".
"There’s been social housing on that site for decades. People need those homes.
"Opposition political parties need to take action to stop this sale," Mr Eddy said.
Board chairwoman Ange McErlain said the fact that social homes that previously existed on the site were demolished made the whole thing even worse.
"They were promised more homes on the site. It’s all really disappointing."
Other former Kainga Ora land for sale by Colliers is the former Aaron Lodge site at 162-164 Kaikorai Valley Rd and 9-17 Brockville Rd, which was once touted by Dunedin Mayor Jules Radich as a possible solution to the homelessness crisis.
"Opportunities of this magnitude and versatility seldom come to the market locally, making this an exciting prospect for developers, investors, or visionaries seeking a large-scale add-value or redevelopment opportunity," the listing said.
"The surrounding area and suburbs are well populated and popular due to their proximity to the city centre, schooling and other amenities. This is a truly unique offering — a blank canvas with multiple possibilities that will appeal to a diverse potential buyer pool."
Earlier this year, Kainga Ora canned 10 separate projects in Dunedin, which would have brought 120 new homes, including a 42-home development in Carroll St in the city centre.
Asked about whether more Kainga Ora land in Dunedin would go on the market, a spokeswoman said decisions to sell specific sites would be ongoing, and at any one time there would be properties at various stages of the process.
"Our focus on renewals means Kāinga Ora will strategically sell some social homes or land it owns. Generally, this will be because selling makes the best economic sense, or we need to prioritise social housing in another area.
"It’s important to note when we sell, we are not reducing our overall number of social homes. For each Kāinga Ora home we sell, we deliver a newly built social home elsewhere."
Labour MP for Dunedin Rachel Brooking said she was particularly sad to see the land sold to private developers, who would make no provision for social housing in the area.
"Once it’s gone, it’s gone — this government could have chosen to provide more social housing for Dunedin, but instead they’ve chosen to ignore this need."
Ms Brooking said she was particularly worried about the Carroll St site, which while not for sale at the moment could very well be soon.
"The whole thing is disastrous. Carroll St was consented and good to go for 42 new homes in a part of Dunedin that had strong connections to all social services.
"It’s just another wasted opportunity."
