Speaking near the site of two former schools in Maskwacis, in Alberta, Francis went even further, apologizing for Christian support of the overall "colonizing mentality" of the times and calling for a "serious investigation" of the schools to assist survivors and descendants in healing.
"With shame and unambiguously, I humbly beg forgiveness for the evil committed by so many Christians against the indigenous peoples," Francis said in the town, whose name means "hills of the bear" in the Cree language.
The 85-year-old pope, who is still using a wheelchair and cane because of a fractured knee, is making the week-long apology tour of Canada to fulfil a promise he made to indigenous delegations that visited him earlier this year at the Vatican, where he made the initial apology.
Indigenous leaders wearing eagle-feather war headdresses greeted the pope as a fellow chief and welcomed him with chanting, drum beating, dancing and war songs.
"I am here because the first step of my penitential pilgrimage among you is that of again asking forgiveness, of telling you once more that I am deeply sorry," he said.
He was addressing the indigenous groups in the Bear Park Pow-Wow Grounds, part of the ancestral territory of the Cree, Dene, Blackfoot, Saulteaux and Nakota Sioux people.
Between 1881 and 1996 more than 150,000 indigenous children were separated from their families and brought to residential schools. Many children were starved, beaten and sexually abused in a system that Canada's Truth and Reconciliation Commission called "cultural genocide."
"I ask forgiveness, in particular, for the ways in which many members of the Church and of religious communities cooperated, not least through their indifference, in projects of cultural destruction and forced assimilation promoted by the governments of that time, which culminated in the system of residential schools," the pope said.
The discovery of the remains of 215 children at a former residential school in British Columbia last year brought the issue to the fore again. Since then, the suspected remains of hundreds more children have been detected at other former residential schools around the country.
Before making his address, Francis, sitting in a wheelchair, prayed in a field of crosses in the cemetery of the Our Lady of Seven Sorrows indigenous Catholic parish and passed by a stone memorial to the two residential schools once in the area.
Survivors and leaders of indigenous communities say they want more than an apology. They also want financial compensation, the return of artifacts sent to the Vatican by missionaries, support in bringing an alleged abuser now living in France to justice and the release of records held by the religious orders that ran the schools.
Some also have called for the Catholic Church to renounce 15th-century papal bulls, or edicts, that justified colonial powers taking away indigenous land.
In January, the Canadian government agreed to pay C$40 billion ($31.5 billion) to compensate First Nations children who were taken from their families.
The Canadian Conference of Catholic Bishops promised to raise C$30 million for healing, culture and language revitalization and other initiatives. The fund has raised C$4.6 million so far.
Pope Francis apologized