Celtic are the first Scottish side to qualify for the Women’s Champions League group stage since it was introduced in 2020-21.
Leading 1-0 from the first leg, headers from Emma Lawton and Shannon McGregor completed the job against Ukrainian side Vorskla Poltava.
Neither side roused the Albert Bartlett Stadium crowd in the first half, though wing-back Lawton stood out following her introduction to Elena Sadiku's starting XI.
A wayward shot on the rebound from Lucy Ashworth-Clifford squandered the home side's finest chance before the interval.
Amy Gallacher spun her marker with ease before curling wide as Celtic piled on the pressure immediately after the restart.
Then Lawton marked a memorable first European start with her first Celtic goal on 52 minutes, the wing-back meeting a cross from Ashworth-Clifford with a towering finish.
A second powerful header would double the hosts' lead on the night as summer signing McGregor nodded in from a Murphy Agnew delivery.
Celtic's historic night was capped off by a clean sheet - despite late threats from Vorskla forward Viktoriia Radionova. The 19-year-old was denied by a Maria McAneny block before firing just over as time wound down in Airdrie.
Celtic will find out their group opponents in Friday's lunchtime draw.
While they are the first Scottish team to enter this phase of the competition, Glasgow City twice reached the quarter-finals in the previous knockout format.