The council is a non-governmental organization that acts as the cultural department of the British Embassy and offers cultural and exchange programs.
The council has come under pressure over the last several years from Russian authorities who claim it is a for-profit organization subject to taxation.
Foreign Ministry spokesman Mikhail Kamynin said in a statement that the suspension of council operations in St. Petersburg and Yekaterinburg was ordered because of "the lack of a legal basis." He said the operations in those two cities were in violation of the Vienna Convention on Consular Relations.
But Natalia Minchenko, marketing director for the British Council's main Moscow office, denied that contention and told The Associated Press that "we have no plans to shut down" the regional offices.
British Embassy officials were not immediately available for comment.
Relations between Moscow and London have been tense.
Britain this year called for Russia to extradite Andrei Lugovoi, whom it identifies as the main suspect in the 2006 killing in London of dissident former security agent Alexander Litvinenko. Russia says its constitution prohibits it from doing so.
Russia, in turn, is furious at Britain for refusing to extradite tycoon Boris Berezovsky, a fierce Kremlin critic, and Chechen separatist envoy Akhmed Zakayev. Both men have been granted political asylum in Britain.
In July, Britain expelled four Russian diplomats in protest of the refusal to extradite Lugovoi. Russia countered by ordering four British diplomats to leave.
The order also demonstrates Russia's general suspicion of foreign non-governmental organizations. Many officials accuse them of meddling in the country's politics and even of attempting to organize opposition movements to try to undermine the government.