May, who is in Japan on an official visit, is reportedly only the second foreign leader to attend a meeting of the National Security Council after Australia's then-prime minister Tony Abbott in 2014.
The Council, which was created at the end of 2013, consists of Prime Minister Shinzo Abe and key ministers.
"Just two days ago, North Korea again went ahead with a reckless act of firing missiles, this time over Japan, and I do hope Japan and the United Kingdom can work together to deal with the threat" from Pyongyang, Abe said at the start of the meeting.
May described Japan as "the UK's closest security partner in Asia" and a "like-minded partner".
"We must work together to enhance our collective response to the threats to the international order and global peace and security," she said.
"That must include confronting the threat that North Korea poses and ensuring that this regime in North Korea stops its aggressive acts."
Britain wants new United Nations sanctions against North Korea that would target guest workers sent mostly to Russia and China, and whose wages are a source of revenue for Pyongyang.
Early today, May visited a naval base on the outskirts of Tokyo with Defence Minister Itsunori Onodera before attending a business forum and the security meeting.
"We have a long history of cooperation in these areas," May said.
"And by the visit today it gives a sign of the growing cooperation and partnership that we have on defence."
Japan's defence ministry on Thursday said it would request its largest-ever annual budget to beef up its missile defence systems.
She will hold a joint press conference with Abe today evening and meet Emperor Akihito on Friday before leaving.
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