The suspected white supremacist allegedly carried out the June 17, 2015 massacre with a .45 caliber Glock handgun at the Emanuel African Methodist Episcopal Church in Charleston after he took part in an evening Bible study class.
Also known as "Mother Emanuel," the church is one of the oldest black congregations in the American South, with strong links to the fight against slavery and segregation.
Police swiftly identified him from a surveillance video and arrested him the next day.
The authorities found chilling evidence of Roof's apparent neo-Nazi leanings on a website believed to be his. He espoused racist views toward African-Americans and posed for photos with firearms and the Confederate battle flag.
Speculation over Roof's case is focused on whether he will receive a sentence of life in prison or death.
"The nature of the alleged crime and the resulting harm" compelled the US Justice Department to pursue the death penalty, US Attorney General Loretta Lynch said.
A separate state trial, which could also result in a death sentence, is expected to begin in January.
As Monday's proceedings get underway, national attention will turn to Charleston, a bucolic port city known for its cobblestone streets and pastel antebellum homes.
Roof is the first suspect who will be considered for potential death sentences at both the state and federal levels, Robert Dunham, the executive director of the Death Penalty Information Center, said.
"The irony is that an institution that has a history of discrimination" against African-Americans, he added of capital punishment in the United States, "is being used to execute somebody for a hate crime.
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