The agreement, signed after talks between Putin and Japanese Prime Minister Taro Aso, opens the door for cooperation in the field of nuclear fuel cycle services and the construction of nuclear power plants.
A number of banking and business agreements were also signed during Putin's visit.
Putin arrived in Tokyo on May 11 for talks with the Japanese leadership, including on a long-standing territorial dispute and economic, energy and international issues.
Russia's nuclear chief said that the signing of the intergovernmental civilian nuclear power agreement would clear the way for Russia to supply low-enriched uranium to Japan worth hundreds of millions of U.S. dollars.
"Today an intergovernmental agreement on cooperation in the peaceful use of nuclear power will be signed, which will give us the opportunity for full-fledged cooperation," Sergei Kiriyenko, part of a delegation accompanying Putin during his visit to Japan, said.
"This deal will allow us to give the green light to projects worth billions of dollars," he added.
Kiriyenko also said that the deal adhered to nonproliferation agreements. "We adhere to the nonproliferation regime with all countries we work with."
Putin said that Moscow and Tokyo could resolve the South Kuril Islands territorial dispute by building mutual trust and developing strong economic ties.
Russia and Japan have yet to sign a formal World War II peace treaty due to their territorial dispute over the four South Kuril Islands, a former Japanese territory annexed by the Soviet Union toward the end of WWII.
"Our mutual work will allow us to resolve a number of global issues, including the signing of a peace treaty [between Russia and Japan]," Putin told a Russian-Japanese business forum in Tokyo.
"Cooperation in the energy sector, which plays a key role in steady supplies of fuel-carriers to the Asian-Pacific region and strengthening the global energy security, remains our priority," he added.
Japan is one of Russia's major trading partners in Asia, ranking third in terms of bilateral trade. Last year, trade turnover between Russia and Japan totaled almost $29 billion.
Japanese companies are currently taking part in two major energy projects in Russia's Far East - Sakhalin-I and Sakhalin-II.