Prime Minister Fumio Kishida vowed to "resolutely defend Japan's territory" as Tokyo lodged a protest with Moscow after a Russian patrol plane entered its airspace.
The military responded by scrambling fighter jets and issuing radio and flare warnings, Defence Minister Minoru Kihara told reporters, calling it the first confirmed incursion since 2019.
"We confirmed today that a Russian Il-38 patrol aircraft has violated our airspace over our territorial waters north of Rebun Island, Hokkaido, on three occasions," Kihara said on Monday.
"Today we lodged a very serious protest with the Russian government via diplomatic channels and strongly urged them to prevent a recurrence."
Kishida, speaking to Japanese media in New York, called the incident "extremely regrettable".
"We will resolutely defend Japan's territory, territorial waters, and airspace," the prime minister said.
Japan has supported the Western position on Ukraine, providing Kyiv with financial and material support and sanctioning Russian individuals and organisations after Moscow's invasion of its neighbour.
Kishida met Ukrainian President Volodymyr Zelensky on Monday on the sidelines of the UN General Assembly.
Zelensky thanked Kishida for his support since Russia's invasion and conferred upon him a top Ukrainian order of merit, Japan's foreign ministry said.
In 2023, an aircraft believed but not confirmed to be Russian entered Japanese airspace, according to Tokyo's defence ministry.
Kihara said the new incident was "the first publicly announced airspace incursion by a Russian aircraft since June 2019", when a Tu-95 bomber entered Japanese airspace in southern Okinawa and around the Izu Islands south of Tokyo.
Earlier this month, Japan had to scramble fighter jets when Russian aircraft flew around the archipelago for the first time since 2019.
The Tu-142 planes did not enter Japanese airspace but flew over an area subject to a territorial dispute between Japan and Russia, Tokyo said.
Russian and Chinese warships recently held joint drills in the Sea of Japan, part of a major naval exercise that Russian President Vladimir Putin said was the largest of its kind for three decades.
Japan scrambled fighter jets in August after the first confirmed incursion by a Chinese military aircraft into its airspace, with Tokyo calling it a "serious violation" of its sovereignty.
Then last week, a Chinese aircraft carrier sailed between two Japanese islands near Taiwan for the first time. Japan called that incident "totally unacceptable from the perspective of the security environment of Japan and the region".
China said the passage complied with international law.