From Thursday morning to afternoon, the Russian Tu-142 aircraft flew from the sea between Japan and South Korea towards the southern Okinawa region, according to a defence ministry statement.
They then travelled north over the Pacific Ocean and finished their journey off the northern island of Hokkaido, it added.
The planes did not enter Japanese airspace but flew over an area subject to a territorial dispute between Japan and Russia, a ministry official told AFP on Friday.
"In response, we mobilised Air Self-Defence Force fighter jets on an emergency basis," the statement said.
The last time Russian military aircraft circled Japan was in 2019, the official said, but that incident involved bombers that did enter the nation's airspace.
Earlier this week, Russian and Chinese warships began joint drills in the Sea of Japan.
The drills are part of a major naval exercise that Russian President Vladimir Putin has described as the largest of its kind in three decades.
Russia and China have ramped up military cooperation in recent years, with both railing against what they see as the US domination of global affairs.
They declared a "no limits" partnership shortly before Moscow launched its offensive in Ukraine in 2022.
Japan also scrambled fighter jets in late August when a Chinese military aircraft "violated" its airspace, according to the defence ministry.
The two-minute incursion into Japanese airspace by the Y-9 surveillance aircraft was the first ever by a Chinese military plane, local media reported at the time.
Since the start of the Ukraine conflict, relations have deteriorated sharply between Japan and Russia, which both claim the Kuril Islands -- known in Japan as the Northern Territories.
The Soviet Union seized the strategically located volcanic archipelago north of Hokkaido in the final days of World War II, and has maintained a military presence there ever since.
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