Brother Number Two Nuon Chea said he had been working for the benefit of his country But Nuon Chea, Pol Pot's deputy, said he had worked to "serve the interests of the nation" by protecting it from colonialism and invaders.
The trial opened on Monday in Phnom Penh.
Nuon Chea, who was also known as Brother Number Two, is being tried alongside Khieu Samphan, the Maoist regime's former head of state, and Ieng Sary, its former foreign minister.
Up to two million Cambodians died of starvation, overwork and execution during the four years of Khmer Rouge rule.
The regime wanted to create an ideal communist society by forcing city residents to work as peasants in the countryside, and by purging intellectuals, middle class people and any supposed enemies of the state.
'Unruly elements'
The Khmer Rouge was led by Pol Pot, who died in 1998. But prosecutor Andrew Cayley said the three defendants could not place all the blame at his door.
"These crimes were the result of an organised plan developed by the accused and other leaders and systematically implemented" by the Khmer Rouge command, he said.
"They cannot be blamed solely on Pol Pot as some of the accused may try."In court, however, says the BBC's Guy Delauney, Nuon Chea painted himself as a defender of the Khmer people - particularly against its larger neighbour Vietnam, which he said wanted to swallow Cambodia "like a python".
In a 90-minute speech, he suggested that "unruly elements" within the Khmer Rouge may have been responsible for atrocities which killed millions of Cambodians.
"My position in the revolution was to serve the interests of the nation and people," he said.
"I had to leave my family behind to liberate my motherland from colonialism and aggression, and oppression by the thieves who wished to steal our land and wipe Cambodia off the face of the Earth."
The trial is only the second to be held at the genocide court. Last year former Khmer Rouge prison chief Duch - who oversaw the notorious Tuol Sleng jail - was jailed for 19 years.
This case against these three men has been broken up into several mini-trials, with the first hearing set to judge on the offence of enforced removal of people from the cities.
This is because the defendants are all in their eighties and concern that they might die has forced the tribunal to split the cases in the hope of gaining at least one conviction.
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