The only previous encounter in the city between footballers representing the two was a pro-unification friendly between the men's teams in 1990, when both used a flag showing the whole Korean peninsula.
Since then, games nominally hosted in the Democratic People's Republic of Korea, as the North is officially known, have had to be played on neutral ground due to authorities' reluctance to see the South's standard fluttering in their capital.
A few hours south of Pyongyang the North Korean military faces off against US-led United Nations forces across the Demilitarized Zone, considered one of the most heavily fortified locations on Earth.
Friday's match came as the North's nuclear ambitions top the agenda at a meeting between US President Donald Trump and his Chinese counterpart Xi Jinping after Pyongyang's latest missile launch this week.
The two Koreas remain technically at war as the 1950-53 Korean conflict ended with an armistice rather than a peace treaty, and relations have plunged in recent months.
Seoul demanded security guarantees for the players before authorities approved the trip, and the South's coach Yoon Duk-Yeo -- who was on the losing side in the 1990 game -- reportedly installed loudspeakers at a training ground to replicate the expected aural barrage.
But the Group B qualifier for the AFC Women's Asian Cup offered a rare chance for a moment of detente between the two.
At the National Art Gallery in Pyongyang - where one room is dominated by a huge painting of the North's women holding aloft the East Asian Football Championship trophy after their victory in 2015 -- a guide said: "It is heartbreaking that we have to participate as two separate teams because our countries are not unified."
A packed crowd at the 40,000-plus capacity Kim Il-Sung stadium stood to hear the South Korean national anthem in respectful silence, before belting out the North's hymn.
In a thunderous atmosphere, every touch by the home team in attack or defence was cheered to the rafters, with supporters waving golden cardboard megaphones in unison.
South Korea's "taegukgi" flag waved gently in the breeze, just a few metres from the North's emblem.
The North, who had home advantage and are ranked 10th in the world by FIFA to the South's 17th, were favourites to win. They have taken the Women's Asian Cup three times and had a head-to-head record of 14 wins, two draws and one loss.
But a missed penalty early on proved costly.
But Jang Seul-Gi netted an equaliser in a 76th minute goalmouth scramble.
Both sides pressed for a winner through seven increasingly tense minutes of injury time, and at the final whistle the South's Taeguk Ladies celebrated as if victorious, while the North's players looked distraught.
Goal difference is now likely to prove crucial in deciding the group winner, who will go through to the AFC Women's Asian Cup finals in Jordan next year.
A Bit Emotional
The football match came after the two countries' women's ice hockey teams played in Gangneung, in the South, on Thursday, with the hosts winning 3-0.
Sporting links "have eased anxieties during times of escalating tensions" said Michael Spavor, director of Paektu Culture Exchange, which facilitates exchanges in multiple fields with the North.
Two gymnasts from the North and South posed for a selfie at the Rio Olympics last year and the image instantly went viral.
When Koreans from both sides of the divide meet, said Spavor, there is "genuine curiosity... and even a little bit of anxiety, which creates a kind of tension".
But at sports events participants "get lost in the moment", he told AFP. "Many athletes realise afterwards how special an experience it was and they can naturally get a bit emotional."
After the match Choe Rim-Hyok, an economics student at KIS university, told AFP that seeing the South's flag and hearing its anthem did not seem strange, as its people were "members of the same nation".
"If our nation is reunified in the near future we can be the most powerful nation in the world," he said.
(Except for the headline, this story has not been edited by NDTV staff and is published from a syndicated feed.)