Keisuke Honda's first-half strike had proved the difference between the sides in this Group C clash up until the 65-minute mark, but quickfire headers from Wilfried Bony and Gervinho turned the game on its head as the Elephants began their tournament with a win.
Buoyed by the inclusion of Yaya Toure - who captained the side in the absence of Didier Drogba, who started on the bench - Sabri Lamouchi's side started brighter and nearly took a sixth minute lead through Bony, whose effort deflected narrowly wide.
Blue Samurai slowly grew into the clash and saw their improvement rewarded on 16 minutes, as Honda's fiercely-struck shot left Barry with no chance.
It could, and perhaps should, have been two just minutes later as wing-back Atsuto Uchida fended off two challenges but fired straight at Barry from a good position.
Ivory Coast emerged from the break the better of both sides but it was not until midway through the half when their dominance saw tangible reward, as Bony's glancing header put the African nation back on level terms.
The comeback was complete minutes later, as Gervinho headed Serge Aurier's cross past Eiji Kawashima, who got two firm hands on the ball but could not prevent it from crossing the line.
Shell-shocked Japan struggled to forge opportunities necessary to level matters, as Ivory Coast held on to seal the win and boost their prospects of progressing from a World Cup group stage for the first time in their history.
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