It is being sold by Graham Wall Real Estate, which also sold the $39 million mansion on Paritai Drive - New Zealand's most expensive house.
Mr Wall said the original 1920s house had been demolished on the Parnell site several weeks ago to make way for the unique development opportunity. The property had a 2011 capital valuation of $8.6 million.
Based on the asking price, the successful buyer would be forking out $4358 per sq m for the undeveloped section, much of which is steep cliff face covered with vegetation.
That compares with $247 per sq m for a 626sq m elevated section in Taupo's Brompton Close with an asking price of $155,000.
QV records show the Parnell section is owned by Stuart Callender and Kerry and Maurice Prendergast, who are linked to the Pumpkin Patch empire. However, marketing material lists the owner as investment company Primo Properties.
The section sold for $8.6 million in June last year. Its capital value was listed as less than $3 million in 2007.
Mr Wall said the section was arguably located on Auckland's best street. He was confident of securing the $10.25 million asking price. His company sold another undeveloped section three doors up for $10 million three years ago, he said.
"This is without doubt the best building site left in Auckland, in my opinion. While it has extraordinary views - you can see from Coromandel to Great Barrier and North Head straight out in front - the real beauty is that it also offers absolute privacy.
"The road is behind you and the views are in front of you. It's a rare thing."
Mr Wall said the property came with two development schemes by Lawrence Sumich architect.
A home deserving of the section could easily cost $8 million to build, he said. "So you could end up with a house and section worth $18 million by the time you've finished."
Mr Wall admitted the dollar figures were well beyond the means of most house hunters. But with prospective buyers for high-end properties flying in from around the globe, there was no doubt New Zealand's real estate market was now truly international, he said.
"We live in the only country on earth with a truly golden future. That's why we're in the international market now."
Meanwhile, the national median house price hit $420,000 last month, a 7.7 per cent ($30,000) increase on the same time last year, and Auckland's median jumped to $614,050.
However the Real Estate Institute says next Saturday's election is putting a dampener on sales, with volumes down 7 per cent in the last month.