Ruto is charged alongside broadcaster Joshua Arap Sang with murder, deportation and persecution all crimes against humanity linked to weeks of savage tribe-on-tribe attacks violence that left more than 1,000 Kenyans dead and forced hundreds of thousands from their homes. Both men insist they are innocent.
Kenyan President Uhuru Kenyatta faces similar charges of helping to orchestrate the violence. His trial is scheduled to start in November.
Ruto's trial is the culmination of years of work by International Criminal Court investigators after Kenyan authorities failed to hold to account any of the leaders of the violence.
While Kenyans once overwhelmingly supported the intervention of the ICC, opinion has turned against the international body, soured in part by the long passage of time.
Kenya's parliament last week passed a voice vote motion to withdraw from the ICC. The vote is symbolic and non-binding; only Kenya's government can decide to withdraw from the ICC and it will have no effect on the trials of Kenyatta and Ruto.
But the vote was carried out by the majority in Parliament, which Kenyan voters put into office in March, the same time they voted in Kenyatta and Ruto, who were under indictments by the ICC. The pair's election campaign had played up the idea that the West was meddling in Kenyan affairs.
The court's registrar, Herman von Hebel, said the motion sent the "wrong message" in the fight against impunity in Kenya.
"Victims of the future should not feel that they are without redress to this court and to international justice," he said.
Rights activists welcomed the opening of the trial as a way of breaking a cycle of violence after recent Kenyan elections.
"For decades those who have turned Kenya's elections into bloodbaths have gotten away with murder," said Daniel Bekele, Africa director at Human Rights Watch. "This ICC trial tackles an impunity crisis in the country and offers a chance for justice denied to Kenyans by their own government."
Ngujiri Wambugu, a prominent social activist in Kenya, once helped collect more than 1 million signatures in support of an ICC intervention, after Kenyan prosecutors failed to bring forward significant judicial action. Today, Wambugu is against the ICC intervention.
"It is quite clear ICC is not being fair," Wambugu said in a column that asked why the leaders of the United States and Britain haven't been indicted for the invasion of Iraq, or why Syrian President Bashar Assad is not being held responsible for the tens of thousands of deaths over the last year in Syria.
That is a sentiment shared across large parts of Africa.
The court so far has indicted only suspects from Africa, leading to charges on that continent that it is biased. The chairman of the African Union earlier this year said that ICC prosecutions "have degenerated into some kind of race hunt."
Kennyatta and Ruto spent the weekend in Kenya's Rift Valley, where hundreds of Kenyan families booted from their homes during the 2007-08 violence still live in shabby United Nations tents. The government gave the internally displaced families a check for about $5,000 each enough to buy a small plot of land in an attempt to close one of the sadder chapters of Kenya's internal violence.
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Straziuso reported from Nairobi, Kenya.