United were at home for their second Tuesday night fixture on the bounce, and manager Paul Simpson made one change to his starting eleven for the first time in five outings.
Dan Butterworth was in for his first league start for the club as Alfie McCalmont missed out of the 18 with a troublesome thigh injury.
Keeper Jokull Andresson had recovered from his illness to take a place on the bench. Meanwhile it was fellow stopper Tomas Holy's 250th senior career appearance.
United were first to show when Back, Garner and Maguire combined by the corner flag, with the latter winning his side a set piece. Moxon delivered, with a rolled pass from a training ground routine, but Butterworth blazed his 19-yard effort high into the Waterworks End.
Maguire started another move when he patiently retained possession on the halfway line. Moxon took over, with a surge, but his low cross was gathered by Crocombe.
The Brewers showed intent on 14 minutes when Helm spread a pass to Carayol. He stepped inside and rifled a stinger at the bottom corner, but Holy got down to beat it away.
United broke, with Back strong in the challenge, and that put Maguire deep into enemy territory. His cross went long and it was shepherded behind to safety. Moxon bent it in but Crocombe stepped back to pluck it out of the air.
Butterworth scampered to the byeline to keep a through ball alive, and his centre achieved just that. Gibson crossed as the ball skittered free, and it eventually came to Back, who had loitered deep. His swerving inswinger was met on the dive by Maguire but he could only find the side netting with the side of his head.
More good work from Butterworth saw him ride two challenges before being stopped in his tracks. The ball was recycled to Moxon, and he kept his shot low with venom. It took a wicked deflection but Crocombe was able to make it stick in his hands at the second attempt, just beneath the bar.
There were half-hearted appeals for a penalty when Guy played Butterworth on with a fantastic pass. A well-timed tackle left the forward on the floor, and the favour was returned when Back won the ball back in the same manner.
But United were caught out moments later when Helm was picked out in space. He took everyone by surprise with a stunning piledriver of a finish that gave the visitors the lead against the run of play.
Carlisle thought they'd equalised when Moxon broke the lines with a measured pass for Butterworth. It looked like he'd missed the opening, but his cut back was excellent. Garner thundered it past Crocombe from close range but Moon counted his lucky stars as it struck his thigh and bounced back out. The defender didn't know much about how, but he'd done his job as form and vital cover.
Burton were dangerous on 38 minutes when Oshilaja ventured into the final third. He had Carayol to his left, and he opened his legs to get his cross away. He put too much on it and it sailed past everybody.
Maguire tried to take matters into his own hands in time added on, with a powerful and accurate shot from distance, but Crocombe was able to parry it into the ground before standing to scoop it up.
Two crosses in quick succession at the start of the second period had Burton stretched, but Powell got enough on the second one to take it beyond Maguire.
Gibson then stepped away from a tight marker to put Armer past his man, but Crocombe came off his line to gather low from the cross.
Substitute Josh Walker used pace to counter but Lavelle was excellent as he kept pace with Powell. The centre back put it behind before any damage could be done.
It was a lovely equaliser in so many ways on 53 minutes, with Callum Guy finding the kind of pass forward that midfielders dream about. Butterworth possibly went for a volley as it dropped over his shoulder, only he will know, but what he did do was put enough on it to give the in-form Jordan Gibson something to be interested in as the ball spun wide. Crocombe got hands to the rasping tight-angled volley but that wasn't enough to stop the attacker's fifth of the season from bulging the net.
Back, Gibson, Butterworth and Gibson were at it again as they clipped their way through the yellow wall with single touches, but the final pass to Maguire was a yard too far behind his boot as he galloped away.
That man Gibson almost did it again just past the hour when he sat deep on a watching brief. Flicks from Lavelle and Guy brought concern for Burton, then the wide man came into play as a half clearance sat up to be hit. Crocombe was in the right place to claim it when it came.
United had what appeared at first sight to be a stunningly well-worked goal chalked off for the ball having gone behind after Armer had beaten his man to overlap and centre from wide. Everybody was celebrating as Back raced in to head it into the gaping net, but the flag was up to signal a corner and the cheering was cut short.
The Brewers were under pressure, but they tried to relieve it when they overturned possession deep in the home half. Walker pulled to the right flank, but he sent a raker of a punt wide as Holy covered his angles.
Persistence all round saw Garner win a header from a throw, and that set Ablade shoulder to shoulder with Seddon. The cross was stopped by Oshilaja, but his hurried clearance was charged down by Moxon. Crocombe had to react smartly to make the save as it came his way.
Guy put a low long-range grasscutter at the keeper as the pace of the game remained at a high tempo, and he somehow stayed upright to get the ball out of his own half to Maguire when it would have been easier to go down. It was then floated to Ablade, but his touch was heavy and the Brewers recovered.
Callum Guy was on it once more on 87 minutes with a sweet through ball that found Ablade. His shot was deflected, but the corner begged to be finished off. Lavelle threw himself at, and couldn't believe it when it whipped over the bar off the top of his boot.
But it was a short-lived reprieve for the Brewers as Ablade rose at the back stick to loop a header back across the face of goal from a Gibson clip. Joe Garner didn't need to be asked twice, and he sent the home crowd wild when he put himself and the ball into the roof of the net.
United closed it down, seeing their way to a thoroughly deserved three points off the back of a strong team display.
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Match Sponsor - Pirelli Tyres Ltd
Match Ball Sponsor - The Kings Head, Carlisle
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Goals
Carlisle United - Gibson (53), Garner (88)
Burton Albion - Helm (28)
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Bookings
Carlisle United - Garner (77)
Burton Albion - Hamer (25), Helm (36), Lubala (77), Maamria (90+1)
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Teams
Carlisle United - Holy, Back (Barclay 88), Lavelle (c), Mellish, Armer, Gibson, Moxon, Guy, Butterworth (Ablade 73), Garner, Maguire. Subs - Andresson (gk), Edmondson, Whelan, Robinson, Plange.
Burton Albion - Crocombe, Seddon (Caprice 81), Oshilaja (c) (Stockton 90), Sweeney, Powell, Moon, Lubala, Helm (Harper 46), Carayol (Gordon 62), Baah (Walker 46), Hamer. Subs - Blackman (gk), Gilligan.
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Match officials
Referee - Ross Joyce
Assistant Referee 1 - Matthew Sowerby
Assistant Referee 2 - Karl Buckley
Fourth Official - Garreth Rhodes
Observer - Graham Salisbury
Coach - Clive Oliver
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Attendance - 6,390 (166)