In a match that also marked the first visit by one of North Korea's football teams to Japan in seven years, the visitors went down 2-1 on Wednesday in Tokyo's national stadium, following a first-leg goalless draw in the neutral venue of Jeddah, Saudi Arabia.
The rekindling of sports ties comes as Japanese Prime Minister Fumio Kishida mulls a meeting with North Korean leader Kim Jong Un in a renewed effort to uncover the fate of Japanese citizens abducted in the 1970s and 1980s by Pyongyang.
It would be the first such face-to-face leaders summit in two decades during which Pyongyang developed nuclear weapons and regularly test fired ballistic missiles into waters near Japan. In 2016, Tokyo banned North Koreans from visiting with exceptions including participants in sport events.
In display of the close but troubled relations between the two countries, the North Korean team was supported by hundreds of cheering fans at the Tokyo stadium, descendants of Koreans brought to Japan as workers, many during World War Two.
Japan, one of the stand-out sides at the 2023 World cup in Australia and New Zealand, proved too good for the visitors in Wednesday's match, Hana Takahashi scoring in the 26th minute.
Aoba Fujino put the match away with a header in the 76th to give Japan their second.
North Korea's Kim Hye Yong scored in the 80th, chipping the ball over keeper Yamashita as she came off her line, but it proved too little, too late for the nation that didn't compete at the Tokyo Olympics in 2021 over fears of their athletes contracting COVID-19.
Japan had much of the possession in the first half with North Korea playing the long ball and counter-attack.
Then Japan withstood North Korean pressure in the first 20 minutes of the second half as the visitors looked for the equaliser.
Takahashi gave Japan a 1-0 lead after her team had much of the early possession. She tapped in a close-range shot after teammate Mina Tanaka's header was deflected off the crossbar by North Korean goalkeeper Pak Ju Mi, the ball falling for Takahashi to score.
North Korea came close to scoring in 44th when Choe Kum Ok's shot was stopped on the line by Japanese keeper Ayaka Yamashita. VAR was not being used in the match but television replays seemed to show the entire ball had not crossed the line.
Japan won the silver in the 2012 Olympics but have never won gold in the women's tournament.