St Stephen's Church has dominated the city's skyline since it was built in 1828.
But falling Church of Scotland attendances saw it close as a place of worship in 1992.
Now, estate agents Rettie are marketing the 23,000 sq ft property for just £500,000.
David Reid of Rettie's said: "It is a fantastic property, with huge potential.
"It is such a striking construction, whenever you are near it your eyes are just drawn to it. Three bedroom flats in the New Town could sell for more than half-a -million pounds and this place is enormous."
St Stephen's, a Category A listed building, was designed by William Playfair, one of Scotland's most revered architects, who also created the National Gallery of Scotland and the Royal Scottish Academy.
It sits at the heart of the Unesco World Heritage site, a fresh vision of city living said to have influenced 18th and 19th-century urban planning all over Europe.
Under existing planning rules, any prospective purchaser could use the three-storey building as a nursery, day centre, museum or library.
But the new owner could also apply for permission to turn it into flats or even the ultimate pied a terre in the capital.