A consistent performance on all six apparatus helped Japan to sneak ahead of early trailblazers the U.S. and take the title with a total of 173.821, just 0.888 of a point ahead of the second placed Americans.
Romania, who had led going into the final round, had to settle for bronze after their title bid came crashing down on the horizontal bar.
Defending champions China paid the price for a stumbling start on the floor exercise and trailed in fifth place.
Japan won the last of their five successive men's team golds in 1976 when the great Mitsuo Tsukahara was among their ranks.
On Monday, it was his son Naoya who proudly showed off his team gold at the Olympic Indoor Hall after the Japanese class of 2004 finally ended years of frustration to claim the ultimate prize in men's gymnastics.
Man of the moment Hiroyuki Tomita, who grabbed the gold with the final routine of the day, said: "This was our first gold in many years but we didn't think about that, we focused on opening a new page for a new Japan."
Having set the standard for the finals by qualifying ahead of favourites China and the United States, Japan's title hopes had initially appeared to be in jeopardy.
OPENING TUMBLE
Tsukahara was first to take centre stage on the floor exercise but he and his two teammates failed to impress the judges and left Japan trailing in seventh place at the end of the first rotation.
With the 6-3-3 format -- in which only three of the six gymnasts from each team compete on any one apparatus and all their scores count towards the team total -- leaving no room for error, the Japanese men knew they had to get back their focus quickly.
As Paul Hamm led the U.S. charge with a dynamic performance on the floor, which included a double-twisting double-layout opening tumble and earned him a score of 9.750, the Japanese men looked on from the sidelines and gave each other encouraging nods.
By the end of the next rotation, Japan had pulled themselves up to third place.
Their effortless scissor movements across the pommel horse drew rapturous applause from the loud Japanese contingent in the arena and a high combined score of 29.075.
Going into the final round, only Romania stood between them and the gold.
But the pressure on the Romanians to win what would have been their first ever men's team gold got to Razvan Selariu who lost his grip during one of his daring release and catch combinations on the horizontal bar and crashed to the mat.
Selariu dragged himself up to complete his routine but his disappointment was etched all over his face. As he hesitantly walked back to his seat, the Romanians knew their chance of glory had evaporated.
Hiroyuki Tomita was the last man to go on the bar and as soon as he nailed his dismount, the Japanese men erupted into wild celebrations even before his mark flashed up on the scoreboard.
"We started out well and our ability to keep going at that level was the deciding factor," a victorious Takehiro Kashima told Reuters.
"We came to Athens with a mission of winning this gold together."
