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The only goal of the game came after just 16 minutes when Paul Shaw fired home with Derby goalkeeper Matt Poom and his defenders appealing for offside.
Derby withdrew Italian Fabrizio Ravanelli with 20 minutes left and the game gave the Rams an early sign of what life will be like in the First Division as John Gregory tries to guide them back to the Premiership at the first time of asking.
Gregory admitted afterwards: "There are going to be 22 more games like this and it's been a real learning curve for us.
"Gillingham worked their socks off to a man against us and we gave away a stupid goal.
"We worked on things like that in training, but one player fell asleep and played everyone on side."
Andy Hessenthaler, nursing cuts to both legs after a competitive night's action in midfield, said: "We didn't have a gameplan as such. We wanted to get at them as quickly as possible and everybody did their job.
"We were relishing playing a team like Derby at this stage of the season but I know that they will do better on their own pitch at Pride Park."
Gillingham might have gone in front earlier than they did with both French strikers Guy Ipoua and new signing Mamady Sidibe a threat in the air and on the ground.
After Shaw had given them the lead Gillingham had another great chance when Hessenthaler set up Sidibe, but the big Frenchman angled his header off target, much to his disappointment.
Derby's best chances came in the first half from Robert Lee and Malcolm Christie. However, Derby's best spell came in the second half when Lee Morris got down the left and his cross found Ravanelli whose shot drifted wide of the far post.
Then a minute later Christie crossed from the left and this time Ravanelli got a touch only for Chris Hope to clear the ball away.
Hessenthaler was booked for the second time in two games and Sidibe also picked up a first half caution while Derby's Adam Bolder and Lee were also yellow carded by referee Steve Dunn.
Ravanelli was taken off with around 20 minutes left in a double substitution, but Gillingham held on to complete a well-deserved win