The Brave Blossoms came from behind at Shizuoka Stadium with Kenki Fukuoka's second-half try and Yu Tamura's boot beating a side recently ranked number one in the world in a shock to match their victory over twice world champions South Africa at the 2015 World Cup.
While they stunned world rugby then, to win this time in front of an uproarious home crowd with so much focus on Asia's first World Cup was arguably more significant.
The hosts were utterly worthy winners and, having admitted that their nerves got the better of them in the 30-10 curtain-raising win over Russia, there was no repeat eight days later.
They came flying out of the blocks and, after Kotaro Matsushima was a bounce away from getting his fourth try of the World Cup, Tamura missed an easy penalty chance to turn 10 minutes of impressive phases into three points.
He would barely put a foot wrong after that.
Once Ireland got a foothold, their game plan became obvious; attacking off the kind of forward pressure that smashed the Scots and testing the Japanese with the clever array of kicking from first five-eighths Jack Carty, starting instead of the struggling Johnny Sexton.
The 27-year-old late bloomer, who started his first test last month and was not part of the Ireland set up until this year's Six Nations, found the dangerous Garry Ringrose with a pinpoint crossfield kick for the first try on 14 minutes and a dink over the top seven minutes later put Rob Kearney in.
Tamura knocked over a penalty in between the two tries and Japan showed the first signs that they were not going away. They had Ireland on the ropes for the remainder of the half, leading to two more Tamura penalties and an exhausted-looking Irish defence happy to hear the halftime whistle to go in 12-9 ahead.
Japan, who had never got within 16 points in seven previous defeats to Ireland, were back at it after the break with more high-tempo attacking play and Ireland already looked like they were hanging on as their penalty count inched up.
Shellshocked, Joe Schmidt's men were making uncharacteristic simple errors and Fukuoka, a last-minute addition to the bench after an injury to Will Tupou, sensationally gave Japan the lead with 20 minutes to go and Tamura slotted over his most difficult kick of the night to make it 16-12.
Ireland, who chose not to risk Sexton after he did not train fully this week, simply had no answer and with the home fans getting louder and louder, Tamura extended the lead to seven points eight minutes from time.
It was never a case of simply hanging on for Japan as they finished the game deep in the Irish half to top Pool A with two wins from two and open up a group Ireland were heavy favourites to top.