The pontiff "conveyed his profound sadness, and that of the Holy See and of the Church, for the genocide against the Tutsi", the Vatican said in a statement following a meeting on Monday, March 22 between Pope Francis and Rwandan President Paul Kagame.
He "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 promote "renewed trust".
In 1994, extremists from the Hutu majority in Rwanda hunted down minority ethnic Tutsis and other Hutus in three-months of killing that left around 800,000 people dead.
The genocide began April 7, 1994, after controversy over the plane crash that killed the then-president of Rwanda, a Hutu.
A dying Rwandan woman tries breastfeeding her child next to hundreds of corpses waiting to be buried at a mass grave near the Munigi refugee camp, where thousands of refugees are succumbing to cholera or dehydration, in this July 23, 1994 file photo.
Several Catholic priests, as well as nuns, were charged with participating in the 1994 genocide. While the killing itself was spearheaded by the Interahamwe militia, everyday people were encouraged, and even in some cases forced, to join the killing.
Francis said he had told Kagame he hoped his apology would help his country heal its wounds.
Singapore and Hong Kong Top Priciest Cities List
While Zurich may be expensive, it compensates by offering a high quality of life that is regularly recognized in other surveys. Zurich, the third most expensive, was the only impediment to Asia holding all top five slots.
Late past year, Catholic bishops in Rwanda officially apologized for crimes committed by the clergy during the genocide.
In President Kagame's 25-minute private meeting with the pope, as well as during his meeting with Cardinal Pietro Parolin, Vatican secretary of state, note was made of "the collaboration between the state and the local church in the work of national reconciliation and in the consolidation of peace for the benefit of the whole nation", the Vatican said.
"Why doesn't he apologise like he does with other cases where more minor crimes were committed by comparison with here?", he said, referring to sexual abuse cases where the pope has regularly apologised to victims and their families.
An official Rwandan statement repeated the government's long-standing accusation of Catholic complicity in the massacres.
Rwanda's foreign affairs minister, Louise Mushikiwabo, also said the historic meeting was characterized by a "spirit of openness and mutual respect".
Athanase Seromba, for instance, a Rwandan Catholic priest, was convicted in 2006 of aiding and abetting genocide and subsequently sentenced to 15 years in prison.
"Today, genocide denial and trivialization continue to flourish in certain groups within the church and genocide suspects have been shielded from justice within Catholic institutions", Mushikiwab said in a statement.