The crab fisherman was shot and killed near Kaigara island, one of several islands off the northeast tip of Hokkaido that are claimed by both Japan and Russia. Russia's regional border patrol said he suffered a "fatal shot in the head."
Russian officials said the man, whose name has not been released, was killed as he rushed to recover fishing tools aboard the 4.9-ton crab fishing boat, No. 31 Kyoshin Maru.
The shooting, linked to a 60-year-old territorial dispute, prompted a series of angry statements between the two nations.
Japan called the act "unacceptable," and demanded immediate compensation and release of the boat and surviving crew, but Russian officials said the captain could face charges for illegally crossing into Russian territory.
Russia's Deputy Ambassador Mikhail Galuzin was quoted by Kyodo News agency as telling Japanese Foreign Minister Taro Aso the boat had violated Russian territory and demanding the breach not happen again. Ministry officials refused to confirm the report.
The four islands - called the Kurils in Russia and the Northern Territories by Japan - were seized by the Soviet army near World War II's end. Tokyo has demanded their return, and the dispute has blocked a treaty formally ending wartime hostilities.
While Russian authorities have seized dozens of Japanese boats and injured several fishermen over the years, this was the first shooting death of a Japanese since October 1956, Coast Guard officials said.