Debutant David Warner hit a quickfire 50 to re-ignite Durham's hopes of making the Twenty20 Cup quarter-finals.
The Australian shared an opening stand of 96 with Phil Mustard (52) as Durham chased down Derbyshire's 153-6 to run out easy six-wicket winners.
Durham now climb up to fourth in the North Division, two points behind Yorkshire and Leicestershire.
Derbyshire's total was built around 59 from veteran Stuart Law, although their innings was interrupted by bright sun.
The east-west direction of the Derby square and the angle of the setting sun combined to make life difficult for the home side and they were unable to make the most of their power play overs, slipping to 19-2.
Greg Smith (22) and Wavell Hinds (23) provided Law with decent support, but Derbyshire's total never looked like being enough from the moment Warner and Mustard started the Durham reply.
Durham were hoping Twenty20 specialist Warner might rescue their campaign and, on this evidence, he may well prove their saviour, smashing a six and eight fours in his 30-ball innings.
He also brought out the best in Mustard, who reached his half century in two balls fewer, with two sixes and four boundaries.
And although Derbyshire also chipped out Kyle Coetzer (16) and Dale Benkenstein (14), Durham got home with two overs to spare.
The defeat all but ended Derbyshire's hopes of reaching the quarter-finals, but Durham now face a crucial home game against Yorkshire on Wednesday night (1730 BST).