Perry Bellegarde says this is a "prime opportunity" for the prime minister to raise the issue.
Stephen Harper is to meet the Pope in the Vatican on Thursday. The meeting comes exactly seven years after the prime minister issued his own apology in the House of Commons to school survivors.
"That would be really symbolic for him to pressure the Pope to formally apologize for the role of the Catholic Church," Bellegarde said in an interview Wednesday. "It would be huge if they do get that apology directly from the Pope."
The Truth and Reconciliation Commission, which was tasked with interviewing thousands of residential school students and documenting their experiences, issued its key findings and 94 recommendations last week. They included a call for a papal apology on Canadian soil.
Bellegarde said that would help bring closure to students who suffered atrocities and abuses at the schools, many of which were run by the Roman Catholic Church.
"People want to hear, 'We're sorry'," he said.
In April 2009, then-AFN national chief Phil Fontaine along with four aboriginal leaders and a delegation from Canada's Catholic Church had a private audience with Pope Benedict in Rome.
The Vatican issued a communique of sympathy after the meeting.
"Given the sufferings that some indigenous children experienced in the Canadian residential school system, the Holy Father expressed his sorrow at the anguish caused by the deplorable conduct of some members of the church," the statement said. "He offered his sympathy and prayerful solidarity."
"It was a delicate matter for the Catholic Church," Fontaine said in an interview Wednesday. "It was a huge undertaking and absolutely incredible achievement ... it was a pretty moving experience."
But he too would now like to see a public apology by the Pope in Canada.
"This is where the experience took place," Fontaine said. "This is where the abuse happened ... An apology delivered by His Holiness on Canadian soil would be of great significance."
Fontaine said he "hopes and prays that the right thing will be done" and that Harper will push for an apology.
The commission's summary report said Pope Benedict's statement of regret was significant to those who were present but it was "unclear what, if any, impact it had on survivors, their families and communities who were not able to hear the Pope's words themselves."
Opposition parties also support the apology recommendation.
Aboriginal Affairs Minister Bernard Valcourt wrote to the Vatican last week to draw attention to the commission's findings.
"Some recommendations relate to the churches which operated residential schools in Canada," Valcourt's letter said. "I wish to bring these recommendations to the attention of the Holy See."