The Justice Department charged James Alex Fields Jr with one count of a hate crime act in the death of 32-year-old Heather Heyer, who died when Mr Fields allegedly drove his car through a crowd of counter-protesters at the right-wing rally last August.
Mr Fields was also charged with 28 counts of hate crime acts causing bodily injury and involving an attempt to kill, and one count of racially motivated violent interference with a federally protected activity. He has yet to enter a plea.
The Ohio native has already been charged in state court with first-degree murder, among other crimes, for which he will be tried in November.
“Last summer’s violence in Charlottesville cut short a promising young life and shocked the nation," Attorney General Jeff Sessions said in a statement announcing the charges on Wednesday. "Today’s indictment should send a clear message to every would-be criminal in America that we aggressively prosecute violent crimes of hate that threaten the core principles of our nation."
Mr Fields was an attendee at last summer's "Unite the Right" rally in Charlottesville, which was billed at the time as the largest gathering of white supremacists in decades. He was seen at the rally carrying a shield for white supremacist group Vanguard America, though the organisation has denied he was a member.
According to a grand jury incitement, Mr Fields returned to his vehicle shortly after police dispersed the rally. He drove down a one-way street where a large crowd had gathered to protest the rally and paused to observe.
The 21-year-old then reversed his car, stopped, and accelerated forward suddenly, according to the indictment. He allegedly ploughed through a stop sign and directly into the crowd of counter-protesters, killing Ms Heyer and injuring several others.
The incident added gravity to an already troubling weekend, during which protesters carried Confederate flags and shouted chants like, "Jews will not replace us!"
President Donald Trump eventually spoke out against the rally, condemning white supremacy but blaming the violence on protesters from "both sides".
Ms Heyer's mother, Susan Bro, told the Huffington Post last year that her daughter's death should be "a rallying cry for justice and equality and fairness and compassion".
“Heather was about bringing an end to injustice," she added. "I don’t want her death to be a focus for more hatred."
Mr Fields' mother, meanwhile, has said she had no idea about her son's political beliefs, and thought he was going to a rally in support of Mr Trump.
Two participants in the "Unite the Right" rally have already been convicted in the beating of a black man in a parking garage near the protest site. Alex Michael Ramos and Jacob Scott Goodwin were both convicted of malicious wounding in the beating of 20-year-old counter-protester DeAndre Harris.
A jury recommended 10 years in prison for Mr Goodwin, and six for Mr Ramos.
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