On-the-whistle report: Derby County 0 Rotherham United 1
The Millers, after losing all seven of their previous games at the Rams' stadium, struck in the 87th minute against a side who began the contest a place above them in the Championship's bottom three.
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Hide AdJamie Lindsay was the hero in a triumph which will build real momentum and belief in their battle to stay up.
Rotherham were worthy of their triumph, having had a Richard Wood goal ruled out by a marginal offside decision in the first half.
England and Manchester United legend Rooney, named boss on the eve of the clash after a spell in interim charge, cut a stern-faced figure at the final whistle.
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Hide AdAfter an even start, Jamal Blackman prevented the Millers falling behind when he was equal to Graeme Shinnie's fierce, ninth-minute drive.
Four minutes later, it was Rotherham who were close to an opener as Matt Crooks' deft pass down the left played in Wes Harding whose low cross was turned wide at the near post by Michael Smith.
Soon after, Matt Olosunde hung the ball up from the right and Ben Wiles powered a header over the bar from 15 yards.
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Hide AdThe Millers were harrying the Rams out of their stride and looking the more dangerous team but Blackman had to be alert in the 26th minute to keep out Lee Buchanan's effort down at his near post.
Paul Warne's men thought they had taken the lead on 35 minutes when centre-half Richard Wood ran in on goal and beat Rotherham old boy Kelle Roos with a finish any striker would have been pleased with only for an offside flag to come to Derby's rescue.
As the interval approached, Kamil Jozwiak skied one over the bar for a home side who had been second best in the first half.
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Hide AdManager Warne had kept faith in the side that had performed so well in a narrow, exra-time FA Cup defeat at Premier League Everton the previous weekend.
That meant Chelsea loanee Blackman kept his place in goal and Viktor Johansson was on the bench after starting the previous three league matches.
Striker Freddie Ladapo was among the substitutes on his recovery from a groin issue and there was a welcome return to the squad for defender Clark Robertson and midfielder Shaun MacDonald following long-term injury absences.
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Hide AdDerby upped their tempo after the break but should have been a man down around the hour mark when Krystian Bielik committed a bookable foul on Crooks but escaped a second yellow card.
Rotherham were relieved to see Martyn Waghorn direct the ball just wide from close range after Kamil Jozwiak had wriggled free on the right before Blackman denied Shinnie for a second time in the contest, holding on to the midfielder's low shot.
Lindsay had a golden chance to snatch victory for the Millers when his 84th-minute effort was cleared off the line by Andre Wisdom.
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Hide AdHis big moment was only another three minutes in coming, though, as Dan Barlaser's free-kick hit the woodwork, wasn't cleared properly and the Scottish midfielder was in the perfect spot to send Rotherham into ecstasy.
Victory lifted them above the Rams in the table into 22nd spot, with only goal difference keeping them in the drop zone.
Goals: Lindsay 87 (Rotherham).
Derby (4-2-3-1): Kelle Roos; Nathan Byrne, Andre Wisdom, Matt Clarke, Lee Buchanan; Krystian Bielik (Max Bird 67), Graeme Shinnie (Louis Sibley 83); Martyn Waghorn, Jason Knight, Kamil Jozwiak; Colin Kazim-Richards. Subs not used: Bradley Foster, Craig Forsyth, Morgan Whittaker, George Evans, Kaide Gordon, Kornell McDonald, Jayden Mitchell-Lawson.
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Hide AdRotherham (3-5-1-1): Jamal Blackman; Michael Ihiekwe, Richard Wood, Angus MacDonald; Matt Olosunde, Dan Barlaser, Jamie Lindsay, Ben Wiles, Wes Harding (Clark Robertson 90); Matt Crooks; Michael Smith (Freddie Ladapo 80). Subs not used: Viktor Johansson, Billy Jones, Curtis Tilt, Trevor Clarke, Shaun MacDonald, George Hirst.
Referee: James Linington (Isle of Wight).