“The Supreme Court has ruled to sustain the claim of Russia's ministry of justice and deem the 'Administrative Centre of Jehovah's Witnesses in Russia' organisation extremist, eliminate it and ban its activity in Russia,” said judge Yuri Ivanenko.
“The property of the Jehovah's Witnesses organisation is to be confiscated to the state revenue.”
A lawyer for the justice ministry, Svetlana Borisova, told the court adherents “pose a threat to the rights of the citizens, public order and public security”.
Judges ordered the closure of the group's Russian headquarters and 395 local chapters, as well as the seizure of its property.
Lawyers for the Jehovah's Witnesses said they would appeal the court's decision, which has not yet come into effect, and could take the case to the European Court of Human Rights.
“We will do everything possible,” Sergei Cherepanov, a Jehovah's Witnesses representative, was quoted as saying by the Interfax news agency.
In 2010, judges in Strasbourg found a previous ruling by a Russian court to ban the organisation unlawful.
The ministry of justice had previously applied for an order to shut down its national headquarters near St Petersburg, state media reported.
Its administrative centre, which has 175,000 members, had previously been suspended in March over alleged “extremist activity”.
Jehovah's Witnesses, who are known for door-to-door preaching and handing out literature, reject some of mainstream Christianity's core beliefs and have more than 8.3 million members around the world.
The US-based group has generated controversy for stances including its rejection of blood transfusions and opposition to military service, facing court proceedings in several countries.
Representatives said hundreds of people gathered at the Russian Supreme Court to hear the six-day case, which they said was the culmination of a decade of “aggressive actions”.
David A Semonian, a spokesman at the sect's world headquarters in New York, said the ministry of justice had “no basis” for its claims.
He said the ban would put members under threat of criminal prosecution even for praying together in a “violation of our basic human rights”.
Jehovah’s Witnesses first registered as a religious group in Russia in 1991 and registered again in 1999, but have been targeted repeatedly by authorities in a wide-ranging crackdown on religious freedom.
Russia changed its legal definition of extremism in 2006, removing requirements for violence or hatred but stating the “incitement of….religious discord” as criteria, leaving the Jehovah's Witnesses with the same legal status as Isis or Nazis.
The group's international website was blocked in Russia two years ago over alleged extremism, with the group's Bibles banned the following year, while a local chairman was jailed for two years on charges of possessing "extremist literature" in 2010.
The Organisation for Security and Co-operation in Europe (OSCE) was among the international bodies condemning a “state sponsored campaign of harassment and mistreatment of Jehovah’s Witnesses” it said dated back to the 1990s in Russia.
It listed police searches, assaults, arson attacks, vandalism, seizures and raids on worship, as well as the arrest of several members and criminal investigations.