The one-day meeting comes as the sides work to end a decades-long territorial dispute that is blocking them from forging a peace treaty. At the same time, Japan, Russia, China and other countries are mulling how best to deal with North Korea's launches of missiles and its nuclear program.
Plans by the US and its ally South Korea to deploy a state-of-the-art missile defence system known as THAAD, meanwhile, have antagonised Beijing and Russia.
Officials on both sides said the talks would largely focus on regional security.
"We will offer our view of the deployment of the US missile defence system in the Pacific region," a Russian Foreign Ministry statement said.
It said joint efforts in fighting terrorism and drug trafficking were also on the agenda.
Japanese Foreign Minister Fumio Kishida began talks with his Russian counterpart, Sergei Lavrov, while Japanese Defence Minister Tomomi Inada will sit down for talks with Russian Defence Minister Sergei Shoigu. The four ministers will also hold joint talks on international and bilateral issues.
Japan and Russia last held "two-plus-two" talks in November 2013. Meetings were shelved after that due to the crisis in Ukraine, as Japan joined sanctions against Moscow.
The Tokyo talks are not expected to lead to a breakthrough on conflicting claims to islands north of Hokkaido - Etorofu, Kunashiri, Shikotan and the Habomai islets - that came under Russian control after Japan's defeat in World War II.
A Japanese foreign ministry official said Tokyo would raise concerns over Russia's instalment of surface-to-ship missiles on Etorofu and other military activity elsewhere on the disputed islands, and seek an explanation from Moscow. It does not plan to push harder than that, said the official, who briefed reporters on the condition he not be named.
Japanese officials said the talks would include work on planning a visit by Prime Minister Shinzo Abe to Moscow later this year. Logistics of visits by Japanese former residents of the disputed islands will also be addressed, they said.
While the countries remain at odds with no clear way forward in resolving the territorial dispute, they are discussing joint development of fisheries, tourism and other areas that might help bridge the gap.