Saki Kumagai scored the winning penalty after Ayumi Kaihori had saved two out of three American three spot-kicks.
Alex Morgan had opened the scoring with a low strike before Aya Miyama poked in the equaliser late in normal time.
Abby Wambach headed USA ahead in extra-time but Homare Sawa ensured a thrilling finale with a spectacular flicked effort at the near post.
The US will be heartbroken and annoyed that they did not manage to secure a record third World Cup having dominated for long periods in the match. But Pia Sundhage's side will rue their profligacy in front of goal, particularly in the first half.
Wambach was the biggest threat in that period and went closest when she crashed a vicious strike against the crossbar following a typical bulldozing run into the area.
Lively winger Lauren Cheney also went close on three occasions. First, she fired just wide at the near post before looping a header over. She then diverted Megan Rapinoe's delightful cross fractions off-target.
Atlanta Beat midfielder Carli Lloyd also should have done better when she smashed her shot over the bar from 14 yards after Shannon Boxx's ball into the area was cleared into her path.
Morgan scored USA's opener
Japan, who had not beaten the USA in 25 meetings - losing 22 of those, looked to catch their opponents on the counter. That tactic paid dividends against hosts Germany in the quarter-final and semi-final opponents Sweden, but the USA defence had dangerwomen Nahomi Kawasumi and Kozue Ando well-marshalled for much of the half.
The surprise finalists did manage to breach the USA area once in the opening half, when fleet-of-foot Shinobu Ohno, playing in her second World Cup, slid the ball into the path of Ando who fell over as she struck what was a tame effort into the hands of goalkeeper Hope Solo.
The second half followed a similar pattern to the first, with USA the more threatening of the two sides.
Forward Morgan, who came on at half-time for Cheney, tried to make her mark within four minutes of setting foot on the pitch, when she stretched out a leg to poke a driven cross against the post.
The pacy 22-year-old had given the USA an alternative target to the physical and aerial threat of Wambach, and in the 69th minute she scored what, at that point, was the most important goal of her young career.
Midfielder Megan Rapinoe, whose delivery was exemplary on the night, launched a 50-yard pass over the top which Morgan latched onto before driving into the box and launching an angled drive past the reach of Ayumi Kaihori.
The youngster was close to tears as she slid to the ground and was embraced by her team-mates.
The USA seemed comfortably on course to victory with Japan dormant as an attacking force.
Sawa scored a sensational equaliser
But with nine minutes remaining the Asian side woke up when Rachel Buehler and Alex Krieger failed to clear their lines allowing Miyama to smash the loose ball past Solo.
The USA were the stronger team in extra time and regained the lead at the end of the first period when Wambach headed in her 13th goal in world cup finals after connecting with Morgan's cross from the left.
But once again, resilient and stubborn Japan equalised when captain Sawa produced an audacious flick from a corner that left keeper Solo helpless.
USA pressed again in search for a late winner. Morgan was en route to scoring her second before she was brought down by Azuza Iwashimizu on the edge of the area, who received a straight red from referee Bibiana Steinhaus.
The free-kick came to nothing which was followed by the whistle to signal the end of extra-time.
A nervous-looking Shannon Boxx set the tone for USA's penalty kicks as she struck her effort straight at Kaihori. The Japanese keeper also saved from Tobin Heath while Carli Lloyd blazed over the bar. Wambach was the only player to find the back of the net but by this stage it was advantage Japan.
Norio Sasaki's side missed one but scored the all-important penalty when young defender Kumagai stayed cool to fire in a brilliant spot-kick high into net.
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