Prosecutors told judges that Bosco Ntaganda committed the crimes while leading fighters of Hema ethnicity on a brutal campaign to drive ethnic Lendus out of the mineral-rich Ituri region in the northeast of the Democratic Republic of Congo more than a decade ago.
The allegations against Ntaganda were made at the opening of hearings in The Hague. The case is regarded as a test for the global legal institution after a series of troubled cases. If convicted, Ntaganda could face life imprisonment. He has yet to enter a plea.
Chief prosecutor Fatou Bensouda said: "[Ntaganda] played a key role in planning assaults against the civilian population in order to gain territory."
Ntaganda, who commanded the United of Congolese Patriots (UPC) militia, had "failed to prevent or punish crimes by troops under his effective command or control", Ms Bensouda told the judges, who will decide if there is enough evidence for Ntaganda to stand trial.
But defence lawyers responded the Ituri conflict had not had the ethnic character that prosecutors were ascribing to it. Defence lawyer Marc Desalliers argued: "The UPC was not a Hema militia. Several commanders belonged to other ethnic groups, including those who took part in the events that form the basis for the charges today.
"The person before you is not Hema, and nor is he from the Ituri region. He grew up in the North Kivu province, he belongs to the Tutsi ethnic group."
Ntaganda is accused of crimes against humanity and war crimes including murder and rape, all allegedly committed during a 2002-03 conflict in the east of the DRC.
"Victims were killed by bullets, by arrows, by nail-studded sticks," said Dmytro Surprun, a lawyer representing victims of the alleged crimes. "Most of them were mutilated, some were decapitated, and their head borne as a trophy."
Ntaganda's lawyers said the militia was defending local civilian populations at a time when Congolese authorities were "absent from the region and even contributing" to the violence. "Taking up weapons to defend people is not a crime; it is a fundamental right," Ntaganda's lawyer Desalliers said.
During proceedings, Ntaganda, a tall, slight man with a pencil-line moustache, spoke only to confirm his identity. He handed himself in to the US embassy in the Rwandan capital Kigali last March after a 15-year career as a commander in a series of conflicts in Ituri province.
Shortly after his arrival in The Hague, prosecutors asked judges for more time to rebuild a case which had been dormant for five years while Ntaganda was on the run.
The session will be a test of prosecutor Bensouda's promise last year that cases will be "trial ready", in contrast to earlier cases that collapsed when judges ruled the evidence was not strong enough.
The court, 11 years old this year, has handed down just one conviction, jailing another Congolese warlord, Thomas Lubanga, for 14 years in 2012 for using child soldiers.
"The court is struggling, and the prosecutor, with her new strategy, has been trying to turn something around," said Bill Schabas, professor of international law at Middlesex University.