The elderly Nuon Chea and Khieu Samphan are the last surviving senior leaders of the Khmer Rouge and are already serving life sentences for the regime's forced transfers and disappearances of masses of people during group's brutal rule of Cambodia in the late 1970s.
Although the widespread slaughter that rent Cambodia between 1975 and 1979 is often called a "genocide" - known as the "crime of all crimes" - the loaded charge carries a narrow legal definition.
The verdict read aloud in the courtroom by Judge Nil Nonn established that the Khmer Rouge committed genocide against the Vietnamese and Cham minorities. It was levelled against Chea and Samphan for the mass murder of Cham Muslim and Vietnamese people, rather than the broader Cambodian population.
The court convicted Khieu Samphan under the joint criminal enterprise rules of the genocide law.
The court has convicted just three people, and many believe Friday's verdict might be the tribunal's last, with Prime Minister Hun Sen - himself a former Khmer Rouge member - claiming that further investigations could threaten stability in the country.
Nuon Chea was brought by ambulance and Khieu Samphan by van from the nearby prison where they are held.
The hybrid court, which uses a mix of Cambodian and global law, was created with the backing of the United Nations in 2006 to try senior Khmer Rouge leaders.
A large crowd of spectators attended Friday's session, including members of the Cham minority.
Lawyers for Nuon Chea said they would appeal, and Khieu Samphan was expected to do the same. "They will always be political and fall short of expectations", said Alexander Hinton, an anthropology professor at Rutgers University and author of two books about the tribunal.
There are fears that politics will thwart the tribunal from undertaking any further prosecutions.
"Today's verdict hopefully brings some measure of justice to the victims, 40 years after the unspeakable mass atrocities committed by the Khmer Rouge in Cambodia", said Nicholas Bequelin, Amnesty International's regional director for East and Southeast Asia.
The two most senior leaders of the the ultra-Maoist group still alive today were convicted in a landmark ruling nearly 40 years after the fall of a bloody regime that presided over the deaths of a quarter of the population.
The Khmer Rouge came to power in the instability that swept through Southeast Asia in the wake of the Vietnam War.
The worldwide tribunal to judge the criminal responsibility of former Khmer Rouge leaders for the deaths of an estimated 1.7 million Cambodians has opened its session to deliver its verdicts on charges of genocide and other crimes.
Scheffer said that "challenges of efficiency, funding, and access to evidence" are issues that plague all worldwide criminal courts, but argued the successes of the Cambodian tribunal should not be diminished.