Manchester City’s third consecutive defeat was the most damaging, a loss that cut deep. Beaten by Manchester United, beaten by Arsenal, they were beaten by Atlético Madrid, knocked out of Europe at the hands of the same team who eliminated them last year.

A late goal from Pauline Bremer set up a frantic final few minutes but in the end a Steph Houghton own goal and a second from Angela Sosa was enough to take Atlético through, 2-1 on the night, 3-2 on aggregate, and end City’s European ambitions.

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For City, twice semi-finalists, this was hard to take and there were tears at the final whistle. “This will hurt,” the manager, Nick Cushing, said. “We’re in a difficult period but we were knocked out a round earlier last year and won two trophies. We haven’t lost three in a row since 2015 but we just need to make sure we keep believing and we will be fine.”

For Atlético, it was historic. They have never been this far in the competition. Their manager, Pablo López, who injured himself jumping about in the tension of the final minutes, said: “It’s amazing, seeing them in the dressing room singing, jumping, dancing. All I can say is thanks for having taken this historic step. I am immensely happy. It’s wonderful to see how happy they are.”

City had needed a goal from the start but did not get it until the 88th minute, their first goal in three matches. By then Atlético had two and City could not add to theirs – although for a few, heart-stopping moments it seemed they might.

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Ellen White was sent through on the left only for her shot to drift wide of the far post for the first chance early on and, soon after, Jill Scott’s effort was blocked. But if that appeared to be a warning, urgency only arrived when the situation became critical and by then it was too late. Cushing said he felt his side had dominated but admitted they could not create meaningful chances and lamented bad luck. “It happens in football,” he said.

Atlético, by contrast, did threaten. A lovely touch from Ludmila da Silva, flicking inside for Sosa, saw her set Toni Duggan away. Shifting the ball on to her right foot, heading horizontally into the area, Duggan was preparing to shoot when the door was closed. From a Sosa corner Ludmila’s header was scrambled away for another one, from which Aïssatou Tounkara could not keep her attempt down.

Then the goal came, five minutes before the break. Sosa found a way out of a crowd, clipping a diagonal ball to the right-hand side for Kenti Robles. She combined with Virginia Torrecilla before sending a long cross dropping behind Gemma Bonner. It seemed to be going out but Ludmila breathed life into the move, keeping the ball from crossing the byline and sending it rebounding off Houghton and into the goal.

Facebook Twitter Pinterest Ellen White of Manchester City is denied by the Atlético goalkeeper Sari van Veenendaal. Photograph: Denis Doyle/Getty Images

City had not scored in their previous two games and Atlético looked the more likely to find the net. City rarely convinced, although a run from deep by Lauren Hemp saw her deliver a superbly weighted pass to White only for Sari van Veenendaal to dive out and block.

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Corral and Ludmila – so direct, so fast, so hard to contain – set up Atlético’s second. Ellie Roebuck had to save at the near post after Charlyn Corral’s sprint up the left. Duggan and Sosa sent Ludmila away, only for her to be dragged down by Megan Campbell. Carmen Menayo hit wide. And then off went Corral again, streaking into the area. Roebuck saved, twice, at the near post but the ball deflected to Sosa, who scored from close range.

A long looping header that could have been the first of the two goals City now needed thudded back off the bar. When they finally did score, it came from a long throw, turned in by Bremer.

Atlético, so comfortable a few minutes before, appeared scared. Another long throw almost led to an equaliser and City’s passage to the quarter-finals but it was the Spanish side who progressed.