The Blues hosted Morecambe at Brunton Park for the second time this season having already met the Shrimps in the Checkatrade Trophy on home turf earlier in the campaign.
United went into the game without defender Anthony Gerrard, who was serving a one-match suspension, and striker Hallam Hope, who was called up to international duty for Barbados.
A minute of applause in memory of Carlisle and Workington favourite Tony Hopper set a respectful tone for the day, with a thank you to the visiting fans who joined with the home supporters to show their appreciation of the life of one of Cumbria's own.
United's first meaningful attack was sparked by a neat turn from Miller just inside his own half. He fed the ball forward to meet a run from Nadesan, but the front man was chopped to the floor as he tried to get past his marker. Sowerby whisked the free kick from wide into the mix but it was just too far in front of the strikers as they bust a gut to try to get on the end of it.
Carlisle kept probing, with Nadesan and Sowerby blocked as they looked to twist into good positions, but there was danger at the Warwick Road End for the Blues when Leitch-Smith reacted first to a loose ball. He turned quckly to shoot but he could only find the side netting.
The hosts broke and Nadesan showed good pace to get onto a rolled pass from Jones as he forged into the box. He shot early, but Roche was there to parry as it flew at him at chest height. Nadesan was first to the rebound but it was awkward and his pull back was gathered by the keeper.
Morecambe stunned their hosts as they took an early lead following some excellent one-touch football which allowed them to drive a path into the area. Collin saved low to his right as he got down to meet a stinger from Leitch-Smith, and midfielder Mike Jones couldn't believe his bad luck when the bouncing ball ricocheted off his boot and bobbled over the line.
Carlisle should have been back on terms when Yates used strength to hold off his man to get into the area. He dropped a shoulder, twice, before popping it across for Bennett to volley. The striker got there but his shot was blocked just as the celebrations were set to start.
Etuhu had a 25-yarder deflected wide as he moved into space to shoot, but the away side did well with the corners that followed. But they were let off the hook when Gillesphey sent a lovely cross towards the penalty area. Nadesan glanced it with his forehead but it bounced back off the upright with Roche well beaten.
Blue shirts stayed forward and Bennett flicked a pass from Sowerby at the back post, again with his head, to where Jones was lurking. The midfielder lost his footing as he shaped to shoot and the moment was gone.
The pace of the game remained fast and Morecambe struck a second blow after an initial header from Oliver had been diverted behind. The big forward was the man on the spot for the corner and he left Collin with no chance as he powered his header into the roof of the net.
Sowerby shot wide from a Nadesan nod down as things started to tighten up, and Collin had to deal with an instinctive volley from Leitch-Smith as the Shrimps continued to look dangerous.
Roche stooped low to gather a header from Bennett as United kept trying to make things happen, and a run from Bennett culminated with a zipped cross which flew across the face of goal untouched as Nadesan battled to make up the ground.
Collin had to parry a thumping effort from Oates as it swirled wickedly in the air, with Morecambe continuing to look the more likely, but Gillesphey was unlucky to see his attempt spoon high as it hit a boot and screwed into the sky. The corner was eventually recycled but Nadesan could only nod a difficult cross from Yates wide as he tried to stretch to get something on it.
The Blues tried to pick the pace up after the break and a good lay-off from Bennett invited Sowerby to shoot. Roche could only parry and it was suddenly there for Bennett to volley, 14 yards out. He swung his leg and the effort was wild. Nadesan was next to test Roche as he went past his man with ease. The angle was tight and the keeper saved with his legs.
Liddle overlapped to put a ball into the area as Carlisle stayed forward for the corner, but Bennett and Nadesan were deep and the ball skidded away off the slick surface. Strong work from Bennett saw him charge a clearance down, and that released Yates as it landed unexpectedly at his feet. He shot early but it hit a defender and curled behind.
United weren't short on corners, but they couldn't make them count as Morecambe threw bodies in the way of the deliveries. Penalty appeals were waved away at both ends as the game opened up, and a mix up between Parkes and Collin gifted Morecambe another set piece from a hopeful punt forward. It was relief all round as Liddle hooked it away.
Morecambe started to slow things down so manager John Sheridan tried to change things from the bench with a triple substitution with just over 20 minutes left to play. Regan Slater almost made an immediate impact as he played a one-two with Yates. His second touch was a goal bound volley but Conlan was there to block.
A mesmerising run from teenager Liam McCarron left three in his wake but his pull back was cut out before Nadesan could strike.
On a day when United said a fond farewell to a much-loved player who had come through the club's ranks, YTS second year Liam McCarron shone through as one for the future as he became the best outlet for an increasingly frustrated home outfit.
That was summed up when Etuhu rifled wide as he lost balance as he looked to get through a gap between Yarney and Mandeville. Yates did much the same as the clock ticked ever faster towards the game's conclusion, and Morecambe shut the doors to lay to claim to an important three points.
Morecambe - Jones (og 13), Oliver (26)
Carlisle United - Collin, Miller, Liddle, Parkes, Gillesphey (Glendon 68), Yates, Etuhu, Jones (Slater 68), Sowerby, Nadesan, Bennett (McCarron 68). Subs - Gray, Brown, Adewusi, Egan.
Morecambe - Roche, Mills, Conlan, Tutte (Cranston 58), Oliver, Yarney, Wildig, Lavelle, Mandeville, Oates (Mendes-Gomes 75), Leitch-Smith (Oswell 82). Subs - Halstead, Jagne, Piggott, Hedley.
Referee - Mr Seb Stockbridge
Attendance - 4,569 (347 away fans)