Debutant replacement flyhalf Kemu Valetini slotted the winning penalty from in front with 80 minutes already up on the clock after a topsy-turvy match played in stifling heat at Churchill Park.
Hammered 61-3 by the 13-times Super Rugby champions in their only previous meeting in May last year, the Drua went 12-0 down early in the contest after the Crusaders scored two tries through rolling mauls.
They stormed back with unanswered tries from centre Iosefi Masi, fullback Ilaisa Droasese, flanker Joseva Tamani and winger Eroni Sau to take a 22-12 lead with 13 minutes remaining.
The Crusaders rallied with a try from Fiji-born winger Sevu Reece and another from a rolling maul for replacement hooker Ioane Moananu, which flyhalf Fergus Burke converted from the touchline to put the visitors 24-22 ahead with seconds to go.
The New Zealanders knocked on from the ensuing kick-off to give the Drua another chance, however, and they worked calmly through several phases before the Crusaders were penalised to give Valetini the chance to secure a famous victory.
"It was unreal today, it was epic," said Drua captain Tevita Ikanivere.
"The boys came out in the second half firing and we did the job, we got the win. We had the belief we could do it and we came and defeated a great Crusaders team.Â
"And what better way to do it than in front of our home crowd."
It was a second defeat in three matches this season for the sometimes slow-starting Crusaders.
"I guess that's not what we wanted, but we got what we expected, that's a tough Drua side playing at home," said Crusaders captain Scott Barrett, who was playing his 100th Super Rugby match.
"We saw how dangerous they were, they capitalised with their skill, running play. Congratulations to the Drua on their win."
