Didier Deschamps' men slipped to a loss against the reigning Asian champions in the last few minutes, after a counterattack capped off a frantic last few minutes in Saint-Denis
Shinji Kagawa converted in from Yuto Nagatomo's cross in the dying minutes, after a succession of misses from the hosts, with the Man Utd midfielder leading the counterattacking charge in the 89th minute and compound the misery, as France slipped up at home for the first time since 2010.
Didier Deschamps had opted for an inexperienced midfield trio of Moussa Sissoko, Blaise Matuidi and Etienne Capoue for the visit of the Asian champions, with Matuidi in particular providing an early attacking threat.
Les Bleus were by far the dominating side of the first half, but as was the case against Belarus in the World Cup qualifier last month, they would be denied by their own profligate finishing, as Laurent Koscielny rose highest to push his header narrowly wide.
Jeremy Menez provided the creative spark, linking well with Benzema, but the Paris Saint-Germain man would indeed see his long range effort fly harmlessly over Eiji Kawashima's bar.
Alberto Zaccheroni's side were floundering, with Deschamps' men utilising the space afforded to them on the wings well, though the interceptions of Maya Yoshida and Yasuyuki Konno denying them the opportunity to break the deadlock in a surprisingly compact period.
Karim Benzema could've had a glorious double within minutes, with the hosts finishing the half strongly. With Menez fouled, the Real Madrid striker curled a wondrous free-kick round the wall, which was then parried away by Kawashima, but not before firing a volley inches wide.
For all of Japan's urgency in defence, they weren't without their own forays in the French half. A speculative cross from the right saw Mike Havenaar's header easily sailing past Hugo Lloris' right post.
The second half brought the customary spate of substitutions, with Deschamps bringing on Clement Chantome, Mathieu Valbuena and Christophe Jallet to aid his flagging side. Giroud headed wide once more, and unable to negotiate past a resolute back four.
At the other end, immediately, Japan were denied by Lloris, who by his accounts endured a rather quiet evening. However, a quick free-kick brought a shot from distance, which the Tottenham goalkeeper initially spilled, before Havenaar failed to connect with the rebound.
Despite the high attacking tempo, and unrelenting pressure from the hosts, they were unable to break down the Asian champions. Valbuena's introduction provided more of a direct service to Giroud, who on occasions, saw his efforts fly wide.
France did have the ball in the net, though the Scottish officials ruled it offside. Valbuena's cross towards Giroud saw the Arsenal striker perform an audacious over-head kick towards substitute Bafetimbi Gomis at the far post who tapped it in bringing premature celebrations to an end.
Amid a frantic finish, neither side could assert their authority, though Giroud should've scored, had it not been for the sublime heroics of Kawashima, whose double save would spark Japan's revival.
From a wasted set-piece, Kagawa surged forward, only for Nagatomo to deliver in a cross, with the former Dortmund winger able to convert past Lloris, and earn Japan a first win over France in their history.
Deschamps' men now travel to the Vicente Calderon to face the reigning world and European champions Spain on Tuesday evening in Group I of World Cup qualifying.