The council, together with Rykneld Homes, secured the funding from the Homes &Communities Agency (HCA) to bring properties up to the Decent Homes standard by 2015.
HCA has allocated £19.7m of the funding for work in 2013/14 and £16.2m for 2014/15.
The Decent Homes work is running alongside a regeneration programme to build the first new council homes in the district for decades, and to refurbish hundreds of other non-traditional properties.
In a joint statement, council leader Graham Baxter and housing chair Betty Hill said: “This represents a huge investment in the future of council housing in North East Derbyshire, and is excellent news for our tenants. This funding will allow us to improve thousands of properties over the years ahead, to provide decent, high quality homes which will be fit for the future.
“Together with the wider regeneration of some of our homes which were built using non-traditional construction, we are now delighted to be in a position to make the biggest investment in council homes for a generation.”