It had looked to be the same old story for Nigel Clough's men as a woeful first half display was compounded by City taking the lead early in the second thanks to a low drive from Martyn Woolford.
But falling behind galvanised the Rams and they levelled six minutes later courtesy of Jamie Ward's incisive run, who set up Craig Bryson to end a run of 334 barren minutes without a goal on home soil.
And a first senior goal for 19-year-old Callum Ball, who had been introduced as a half-time substitute, gave the home side the points in the 73rd minute when he shot under David James.
The victory - their first win in eight games - provided much needed needed respite for Clough and following on from last week's point at Crystal Palace, he will hope it is the start of a Derby resurgence.
The defeat for City, meanwhile, is the second in a row and brings to an end the promising start of Derek McInnes' reign.
Having not won or scored at Pride Park since October 29, Clough will have been demanding his side to put on a show for their fans and end their miserable run of form.
But, for all their possession, his calls were not answered as a dour first half showing ensured they got nowhere near James in the City goal, with the former England goalkeeper virtually redundant throughout the first period.
City, who have been on a decent run of form, were hardly threatening either though, but they did at least force Rams stopper Frank Fielding into a couple of saves.
First he was forced down low to keep Albert Adomah's stinging drive out and then an entirely forgettable first 45 minutes came to a close with a rare moment of quality when Nicky Maynard's fizzing drive from distance was superbly tipped over by the England Under-21 keeper.
City continued on top after the restart and duly took the lead in the 56th minute after Woolford was set free by Adomah's defence-splitting pass and the former Scunthorpe midfielder bagged his first goal for the Robins with a low finish under Fielding.
That goal inspired the Rams and their fans finally had something to cheer six minutes later when they scored their first goal on home soil for over five and a half hours to level.
Ward, who had been the Rams' most promising player, went on a surging run into the penalty area and his cutback from the byline was tapped in at the far post by Bryson.
And the fans only had to wait nine minutes for another celebration as Ball scored his first senior goal when he took Paul Green's shot in his stride and fired low under James, who should have done better.
McInnes' side came within inches of earning a deserved point but Brett Pitman's back-heel went just wide of the post.