Pope Francis has plead for forgiveness for "the sins and failings of the Church and its members" implicated in the 1994 Rwanda genocide that killed about 800,000 people.
Rwanda's President Paul Kagame is welcomed by Pope Francis during a private meeting at the Vatican, March 20.
He begged for God's forgiveness "for the sins and failings of the Church and its members" who, the statement said, had "succumbed to hatred and violence".
Acknowledging the November 2016 apology by the Rwandan bishops, Francis asked that the Vatican's "humble recognition of the failings of that period" could contribute to renewed trust between the Catholic Church and the Rwandan authorities.
The Catholic Church in Rwanda previous year publicly apologised for the actions of some Catholics and priests during the genocide that lasted around 100 days in 1994.
Mr Kagame, Tutsi, led a rebel force to halt the slaughter in 1994 as accusations surfaced that some priests and nuns had taken part in the killings.
Other individual priests have since been convicted of human rights violations for heinous acts during the genocide such as bulldozing a church with 2,000 Tutsis inside and raping Tutsi women.
The highest-ranking Church official to be tried for genocide was the late bishop Augustin Misago, who was acquitted and freed from prison in June 2000.
"The Rwandan government at the time said the apology was 'profoundly inadequate".
A report on the genocide commissioned by the Organisation of African Unity said the church in Rwanda had offered "indispensable support" to the Hutu regime during the killing, and that church leaders had played a "conspicuously scandalous role" in the genocide by failing to take a moral stand against it.
During Monday's meeting, the Argentine pontiff "conveyed his profound sadness, and that of the Holy See and of the Church, for the genocide against the Tutsi", Vatican Radio reported.
The Catholic Church in Rwanda past year offered an apology, saying some of its members had fanned the ethnic hatred that led to the killings, but Kagame said at the time that he wanted the Pope himself to say sorry.
Rwanda's foreign affairs minister Louise Mushikiwabo said today that the Vatican talks between Francis and Kagame were "characterised by a spirit of openness and mutual respect".
Four Catholic priests were indicted by the UN International Criminal Tribunal for Rwanda for their role in the genocide in 2001.
Their statement acknowledged church members planned, aided and carried out the genocide, and that the local church had later resisted efforts by the government and groups of survivors to acknowledge the church's complicity in mass murder.
A number of churches became scenes of mass killings during the 100-day rampage, as Hutu militiamen found people seeking refuge there, sometimes turned over by priests, with no way out.
"It allows us to build a stronger base for restoring harmony between Rwandans and the Catholic Church", she said.