A superb debut goal from Jimmy Bullard and David Norris' eighth strike of the season gave Town a second successive Championship win.
Bullard, who arrived at Portman Road on loan from Hull last week, volleyed past Stephen Bywater to cancel out Alberto Bueno's early opener for the Rams.
Norris twice went close to finding net before he rounded off a neat move midway through the second-half to fire past Bywater and go top of Town's goalcharts - and give Paul Jewell a winning return to the club he managed for a year.
Town made two changes to the side that went down bravely at Arsenal in the semi-finals of the Carling Cup, Lee Martin returning to the side after being cup-tied at the Emirates and Bullard coming in to the middle of the park.
Connor Wickham miskicked on the edge of the box in the opening exchanges before Derby gained the advantage on seven minutes. Gareth Roberts escaped the Town offside trap and crossed from the left, Bueno did the rest from six yards.
Martin posed a threat for Town down either flank, his cross beaten out by John Brayford, then had another delivery cleared by Miles Addison at full stretch.
Carlos Edwards, operating at right-back again, showed good pace to prevent Ben Davies getting into the box, the Trinidad international then testing Bywater with a teasing cross.
The former Town loanee 'keeper did well to keep out Norris' left foot effort but on 28 minutes he was picking the ball out of the net after a sublime volley from Bullard.
Bueno fired over as Derby looked to respond, the Rams' striker then seeing a header drift wide.
Damien Delaney had an anxious look back as the ball skimmed off his head but Marton Fulop was there to make the save, the 'keeper then quickly off his line to kill the danger threatened by Chris Porter as a fairly evenly contested first-half came to an end.
Porter forced a corner as the second-half got underway, Davies then volleying just wide from 25 yards.
Delaney deflected Bueno's effort wide for a corner as the Rams threatened, Shaun Barker heading wide from the flag kick.
Town countered on the hour, Bullard fed Norris on the left of the box and the skipper drilled his shot just wide.
Gareth McAuley closed down the danger from a Roberts cross, Addison doing the same at the other end as Tamas Priskin broke.
Edwards' cross beat everyone except Bywater, Priskin then thwarted as he tried to feed Wickham but seconds later Town got the breakthrough, Priskin setting up Norris who found the net with a left foot drive on 68 minutes.
Barker picked up the first yellow card of the game for a foul on Norris, Derby then making a first change with Steven Davies on for Porter for the last 20 minutes.
Green made way for Tomasz Cywka in the Rams' second change. Edwards was booked a foul on the edge of the Town box, Davies' free-kick deflected wide.
Fulop flicked over another Davies free-kick in added on time, then dealt with a corner but Town held on for the points and a first away win under Paul Jewell's management.
Derby: Bywater, Brayford, Roberts, Barker, Addison, Green (Cywka 78), Pearson, Bailey, Davies, Bueno, Porter (Davies 71). Subs not used: Savage, Deeney, Pringle, Doyle, Hendrick. Booked: Barker.
Town: Fulop, Edwards, McAuley, Delaney, Kennedy, Norris, Leadbitter, Bullard, Martin, Wickham, Priskin. Subs not used: Peters, Scotland, Lee-Barrett, Smith, Healy, Civelli, O'Dea. Booked: Edwards.
Att: 23, 159