In a statement Catholic bishops admitted they'd "killed each other" and said sorry "on behalf of all Christians".
Hutus, the ethnic majority, murdered hundreds of thousands of minority Tutsis, as well as moderate Hutus who opposed the massacre, over a 100-day period.
It's since been revealed the genocide was instigated by the Hutu-majority government of the time with the Catholic Church being complicit and some murders taking place in churches.
Some survivors say nuns and priests also murdered people themselves.
The Conference of Catholic Bishops said: "We apologise for all the wrongs the church committed. We apologise on behalf of all Christians for all forms of wrongs we committed. We regret that church members violated [their] oath of allegiance to God's commandments.
"Forgive us for the crime of hate in the country to the extent of also hating our colleagues because of their ethnicity. We didn't show that we are one family but instead killed each other."
Callum Henderson, director of the Christian charity Comfort Rwanda and Congo, told Premier's News Hour this apology had been "a long time coming."
Asked why it hadn't come sooner, he said: "It's really the whole idea that the Church can't be held responsible for the actions of individual members and an unwillingness, really, to accept corporate responsibility in that sense.
The apology coincides with the formal end of the Catholic Church's Holy Year of Mercy, with finished on Sunday.
Speaking about the scale of involvement by members, Callum Henderson also said: "You had some Catholic members who were very brave, and who protected and care for Tutsis who were being hunted in the genocide. You have everything from that through to clergy, in particular, who called in the militia.
"There has been a process of forgiveness, healing and reconciliation going on in Rwanda now for a number of years; very, very positive and a real miracle of God in many sense, where perpetrators and survivors are brought together."
