Russia 2018 will be their sixth successive appearance at a World Cup, with the legacy of hosting the tournament alongside South Korea in 2002 living on with the current crop of players.
Japan have so far alternated between a group-stage exit and reaching the knockout rounds in each tournament, and they will be hoping that pattern continues this summer having been eliminated without winning a game in Brazil four years ago.
Here, Sports Mole assesses Japan's chances at the World Cup in Russia.
The draw could have been worse for Japan, who avoided any of the major World Cup heavyweights when they were placed alongside Poland, Colombia and Senegal in Group H.
Japan will nonetheless be up against it as the lowest-ranked team in the group, and they will likely need to pull off an upset somewhere along the way if they are to prevent favourites Poland and Colombia from claiming the top two places in the group.
Should they manage to avoid defeat in their opening match against Colombia then that could set them up nicely for their easiest game on paper against Senegal next up, before ending the group stages against Poland.
June 19: Colombia vs. Japan (1pm, Mordovia Arena, Saransk)
June 24: Japan vs. Senegal (4pm, Central Stadium, Yekaterinburg)
June 28: Japan vs. Poland (3pm, Volgograd Arena, Volgograd)
HOW THEY QUALIFIED
Japan's qualifying campaign began all the way back in June 2015 with a less-than-convincing goalless draw at home to Singapore, but from then on they did not look back.
The team - then managed by Vahid Halilhodzic - won their next seven games without conceding a single goal, ensuring that they cruised through the first phase of qualifying in style, scoring 27 goals without reply along the way.
Predictably, the second phase was not as straightforward, and fans may have been fearing the worst when it began with a 2-1 defeat at home to UAE, squandering a lead in Saitama on their way to the loss.
It proved to be another case of Japan being slow starters, though, and they went on to take 20 of the next 24 points available to them to gain control of the group.
A 2-0 win over Australia in August 2017 sealed their place in Russia, meaning that a final-day defeat to Saudi Arabia was inconsequential as far as Japan were concerned.
New manager Nishino has had just three friendlies to drill his side since his appointment in April, and results have not been all that convincing.
Japan suffered a 2-0 loss to Ghana at the end of May and lost by the same scoreline to Switzerland a week later, but their winless and goalless run did come to an end in their final warm-up match.
Takashi Inui netted twice in a 4-2 victory over Paraguay in Austria on Tuesday, giving a previously disciplined Japan side a much-needed boost before jetting off for their sixth successive finals appearance.
Even if results have not been perfect, the Samurai Blue have at least managed to fit in games against African, European and South American opposition over the past few weeks, giving them some practice ahead of those matches that really matter in Russia.
Goalkeepers: Eiji Kawashima (Metz), Masaaki Higashiguchi (Gamba Osaka), Kosuke Nakamura (Kashiwa Reysol).
Defenders: Yuto Nagatomo (Galatasaray), Tomoaki Makino, Wataru Endo (Urawa Reds), Maya Yoshida (Southampton), Hiroki Sakai (Marseille), Gotoku Sakai (Hamburg), Gen Shoji, Naomichi Ueda (Kashima Antlers).
Midfielders: Makoto Hasebe (Eintracht Frankfurt), Keisuke Honda (Pachuca), Takashi Inui (Eibar), Shinji Kagawa (Dortmund), Hotaru Yamaguchi (Cerezo Osaka), Genki Haraguchi, Takashi Usami (Fortuna Dusseldorf), Gaku Shibasaki (Getafe), Ryota Oshima (Kawasaki Frontale).
Forwards: Shinji Okazaki (Leicester), Yuya Osako (Werder Bremen), Yoshinori Muto (Mainz).
STAR PLAYER - Makoto Hasebe
Shinji Okazaki and Shinji Kagawa made the cut for the 23-man squad, despite being overlooked for selection from November until the summer.
How big a part they will play under the new boss Akira Nishino remains to be seen, meaning that it is down to other, perhaps less-familiar faces, to make a name for themselves in Russia.
Makoto Hasebe is now a real veteran on the international stage, having racked up more than a century of caps for the Samurai Blue since 2006, and he has an important role to play in defensive midfield in what will surely be his last World Cup.
The Eintracht Frankfurt ace has experience of skippering his side at major tournaments and, in one of the competition's more disciplined teams, he is tasked with keeping things ticking over in the engine room.
MANAGER - Akira Nishino
Akira Nishino has been tasked with something of a rescue job in charge of the national team, having been appointed just 70 days before the start of their campaign in Russia.
Halilhodzic's sensational sacking in April was put down to his relationship with the players, leaving Nishino just over two months to repair the damage and attempt to replicate his time in charge of Japan's youth teams from the 1990s.
The 63-year-old's most notable coaching achievement at that level saw him steer Japan to victory over a Brazil team containing Ronaldo and Roberto Carlos at the 1996 Olympic Games, while at club level he enjoyed a particularly trophy-laden nine-year spell with Gamba Osaka, leading them to their only ever AFC Champions League title and a third-place finish at the FIFA Club World Cup later that year.
Nishino also won 12 caps for his country during his playing career, despite his time in the Japan team spanning just 1977 and 1978.
WORLD CUP RECORD
Best finish: Last 16 (2002, 2010)
Japan were not able to match the momentum South Korea enjoyed in front of their home crown in the jointly-hosted 2002 tournament, but they did still record their best-ever finish at a World Cup by reaching the last 16.
After topping a group which included Belgium, Russia and Tunisia, Japan were beaten by Turkey in the last 16 to see their campaign come to an end on home soil.
There was penalty shootout heartbreak against Paraguay in the last 16 eight years later on the only other occasion in which Japan have made it out of the group stages.
Four years ago Japan finished bottom of a group which coincidentally also included Colombia, and they suffered the same fate in 2006 and 1998, the latter of which saw them lose all three group games on their debut appearance at the tournament.
Overall Japan have played 17 World Cup matches, winning four of those with four draws and nine defeats while scoring 14 goals and conceding 22.
Japan may have avoided any genuine heavyweights in their group, but they still have their work cut out and, considering their disrupted build-up, they would do well simply to stay off bottom spot in Group H.
VERDICT: Fourth in Group H