Captain Makoto Hasebe opened the scoring for the three-time champions in the 35th minute, but Syria pulled one back from a penalty controversially awarded against goalkeeper Eiji Kawashima on 76 minutes.
Kawashima was adjudged to have brought down Sanharib Malki despite the player being flagged offside. Japanese players and team officials protested loudly but Iranian referee Torky Mohsen gave a penalty and dismissed the goalkeeper in chaotic scenes.
Shusaku Nishikawa came on as a replacement and the first thing he had to do was pick the ball from the back of the net after Firas Al Khatib calmly converted the spot kick. Down to 10 men, Japan nevertheless stepped up a gear and their FIFA World Cup™ hero Keisuke Honda slotted in the winner from another penalty six minutes later.
"The referee's decision was wrong," Japan coach Alberto Zaccheroni said. "We confirmed the linesman raised the flag but the referee ruled it was not an offside, saying that the ball was in the process of a Japanese back pass," said the former AC Milan boss. "We will check the video again."
Syrian's Romanian coach Tita Valeriu hit back: "I agreed that the red card against the Japanese goalkeeper was correct." This goalkeeper deserved that red card because our player was alone at the back and he hindred him."
But Zaccheroni, leading Japan's bid to regain the title they lost in 2007, said he was satisfied with the way Japan played. "It was totally a one-sided game for Japan," he said. "Our 10 men worked as if they were 11. They fought gallantly."
Japan badly needed the three points to live up to their credentials after salvaging a 1-1 draw with Jordan in their opener. Jordan beat Saudi Arabia 1-0 in the earlier Group B game to put the Gulf giants out of contention, with Japan and Jordan now on four points, Syria on three and the Saudis down and out on zero.
The Blue Samurai, who reached South Africa 2010's last-16 round in June, struggled to penetrate a tight Syria defence at the outset. They all but opened their account in the 11th minute when leading J-League striker Ryoichi Maeda headed a right cross from Atsuto Uchida in front of goal but the ball swerved onto the left side of the net.
Japan started to find more rhythm but squandered a chance on 34 minutes when Yasuyuki Konno's back header on an Endo corner was stopped by Syrian goalkeeper Mosab Balhous. But a minute later Hasebe opened their account with a beautifully placed right-footer from just inside the box on a cross from Daisuke Matsui after some good work by Honda.
Honda dribbled deep into the right side of the area and hooked a cross to Matsui who turned around to feed the ball to Hasebe.
Maeda attempted two close-range shots within five minutes just before half-time, shooting off the left post and heading over an Endo corner, as Japan turned up the heat.
After the break, Syria started to fight back, with Mohamad Al Zino having a decent chance on 55 minutes. In 62nd minute, Al Dyab connceted with a Al Khatib corner but his header bounced into Kawashima's arms.
Soon after the Lierse SK custodian was sent off for the controversial penalty, but Japan showed character to win the match in the 82nd minute when Ali Dyab pulled down substitute striker Shinji Okazaki. Honda stepped up to bury the ball in the back of the net.
A desperate Syria threw everyone forward in a bid to find the equaliser but despite six minutes of extra time they left the pitch empty-handed.