The Pope has begged forgiveness for the "sins and failings of the church and its members" during Rwanda's 1994 genocide and told Rwanda's president that he hoped his apology would help the country heal.
In an extraordinary statement after Francis' meeting with President Paul Kagame, the Vatican acknowledged that some Catholic priests and nuns "succumbed to hatred and violence, betraying their own evangelical mission".
The Vatican said Francis also "expressed the desire that this humble recognition of the failings of that period, which unfortunately disfigured the face of the church, may contribute to a 'purification of memory' and may promote, in hope and renewed trust, a future of peace".
The Vatican's statement followed an official apology issued last year by Rwanda's Catholic bishops.
During the 100-day genocide, more than 800,000 ethnic Tutsis and moderate Hutus were killed by Hutu extremists.
Many of the victims died at the hands of priests, clergymen and nuns, according to some accounts by survivors, and the Rwandan government said many died in the churches where they had sought refuge.
The Rwandan government has long pressured the church to apologise for its complicity in the genocide, but both the Vatican and the local church have been reluctant to do so.
The church has long said those church officials who committed crimes acted individually.
In 1996, St John Paul II refused to take blame on the church's part for what transpired in Rwanda, saying in a letter to Rwandan bishops: "The church in itself cannot be held responsible for the misdeeds of its members who have acted against evangelical law."
Four years later, however, he did make a general apology for a host of Catholic sins and crimes over its 2,000-year history.
Amid continued pressure from the government, Rwanda's Catholic bishops last year apologised for "all the wrongs the church committed".
The ministry of local government rejected the apology then as inadequate.
During Rwanda's annual dialogue in December, Mr Kagame said he did not understand why the church was so reluctant to apologise for genocide when popes have apologised for other crimes.
"I don't understand why the pope would apologize for sexual offences, whether it is in the US, Ireland or Australia, but cannot apologise for the role of the church in the genocide that happened here," Mr Kagame said at the time.
On Monday, the Rwandan government called Francis' meeting with Mr Kagame a "positive step forward".
"Today's meeting was characterised by a spirit of openness and mutual respect," said foreign minister Louise Mushikiwabo.
"It allows us to build a stronger base for restoring harmony between Rwandans and the Catholic Church."
However, Ms Mushikiwabo repeated charges that even before 1994, Catholic institutions helped divide Rwandans and "laid the intellectual foundation for genocide ideology".
"Today, genocide denial and trivialisation continue to flourish in certain groups within the church and genocide suspects have been shielded from justice within Catholic institutions," the statement said.