At issue before the province's top court is whether the aboriginal men were treated shabbily because on-reserve First Nations people were excluded from the juries that convicted them.
"Our society has proven to be very efficient at charging First Nations and jailing First Nations," said defence lawyer Julian Falconer.
"We don't seem so good at constructively involving First Nations in the justice system, such as their participation in the jury system."
Last summer, the Ontario Court of Appeal upheld a manslaughter conviction against Clifford Kokopenace as reasonable.
However, in an unusual twist, the court put the ruling on hold in light of the constitutional challenge sparked by the jury-representation issue.
A non-aboriginal jury in Kenora, Ont., convicted Kokopenace in 2008 of stabbing a friend to death on the Grassy Narrows reserve.
Also involved in the Appeal Court hearing is Clare Spiers, an aboriginal with a long record of violent crime. He was convicted of first-degree murder in 2007 in Barrie, Ont., for kidnapping a woman and slitting her throat.
No on-reserve residents were among the 286 people offered up for his jury.
An Appeal Court decision in their favour would have implications for how the Ministry of the Attorney General selects potential jurors. It might also offer grounds for similar court challenges.
"Serious questions would arise about convictions based on those same jury rolls," said Falconer, who speaks for the Nishnawbe Aski Nation, which is intervening in the appellate hearing.
The years-long under-representation of aboriginals first came to light at coroner's inquests in northern Ontario into the 2007 deaths of Jacy Pierre, who died in police custody, and teenager Reggie Bushie, who drowned.
The issue paralyzed jury proceedings — criminal, civil and inquest — in the region, as judges put other murder and fraud cases on hold.
For its part, the Ontario government argues an accused has no "absolute right" to a representative jury.
It also argues that justice officials did their best to ensure representative juries, but was stymied by privacy legislation and lack of co-operation by First Nation leaders.
The Nishnawbe Aski Nation, which represents 49 First Nations communities spread out over an area covering two-thirds of Ontario, argues neither the government's good intentions nor the diligence of court staff is relevant.
"Many of the worst deprivations of First Nations people's rights have been achieved through 'well-intentioned' policies," their factum states.
While Spiers is primarily taking issue with how potential jurors were vetted — an issue expected to take up the first two days of this week's Appeal Court hearing — the question of representation is also at play.
His defence lawyer, Anthony Moustacalis, blames "institutional neglect" for failing to ensure a fair jury-representation process.
"They didn't sample sufficiently for First Nations people who are on reserve," Moustacalis said.
In March last year, Appeal Court Justice John Laskin was highly critical of how the Pierre and Bushie families were stonewalled when they made "reasonable" requests for information on the makeup of coroner's juries.
"They did not get any answers; instead they got a runaround," Laskin wrote. "A lot of time and money might have been saved had the ministry and the coroners simply provided this information."
The issue prompted the Ontario government to set up a judicial inquiry. Former Supreme Court of Canada justice Frank Iacobucci is due to report into by August.