The commission's latest annual report attributes the surge to a 2008 law change that allowed First Nations members to file complaints about matters under the Indian Act, which had been shielded from human-rights scrutiny.
"This is an encouraging and important outcome," David Langtry, the acting chief commissioner, said in a statement.
"The sheer volume of complaints tells us that aboriginal people are beginning to use the Canadian Human Rights Act to improve their lives by holding their own governments as well as the federal government accountable for human rights."
The law change let aboriginal people file complaints against the federal government, which they had previously been unable to do, starting in June 2008.
Then in June 2011, aboriginal people were allowed to complain to the commission about their own First Nations governments.
Since then, the number of complaints has shot up.
Between 2008 and 2011, the commission received fewer than 50 complaints a year from First Nations groups against the federal government. But since 2011, First Nations groups have filed 390 complaints against their own governments and Ottawa.
Of those, 225 complaints were against First Nations governments, mostly over housing issues and eligibility to vote in band council elections. Another 165 complaints were filed against the federal government over funding for education, policing and child welfare.
The commission says a case currently before the Canadian Human Rights Tribunal will be a "major test" of aboriginal people's ability to use human-rights laws.
The case arises from a complaint against the federal government from First Nations child-rights advocates, who claim that Ottawa is short-changing native communities by under-funding child-welfare services.
The human-rights challenge launched by the First Nations Child and Family Caring Society and the Assembly of First Nations dates back to 2007.
But Ottawa has argued that the case should not be heard at all because it's not fair to compare federal programs with provincial programs.
Federal officials also say they have been putting more money into First Nations child welfare and reorienting their programs to focus on keeping families together.
After much wrangling and millions of dollars in legal fees, the Federal Court rejected the government's arguments, ordering a full hearing at the Canadian Human Rights Tribunal.
The government appealed the Federal Court's decision. Earlier this month, the Federal Court of Appeal upheld the Federal Court's decision.
Ottawa still has the option of asking the Supreme Court of Canada to hear its appeal.
Meanwhile, the Canadian Human Rights Tribunal began its hearings late last month.
Billions of dollars are at stake. If First Nations complainants win the case, Ottawa would likely be required to fund social services on reserves at the same level per capita as the provinces fund similar services off reserves.