"By ignoring the warnings of the most lucid observers, France bore overwhelming responsibility in a spiral that led to the worst." Macron is the first Gallic leader since 2010 to visit the East African nation, which has long accused France of complicity in the killing of some 800,000 mostly Tutsi Rwandans.
He went further than his predecessors, saying that only those who had survived the horrors "can maybe forgive, grant us the gift of forgiveness".
However, Macron said France was "not complicit" in the genocide. "The killers who stalked the swamps, the hills, the churches, did not have the face of France. France was not an accomplice," he said.
Egide Nkuranga, of the survivors' association Ibuka, was disappointed that Macron did not "present a clear apology on behalf of the French state". However, he said the speech "really tried to explain the genocide and France's responsibility. It is very important. It shows that he understands us."
Paul Kagame, Rwanda's president, said: "His words were something more valuable than an apology. They were the truth. Speaking the truth is risky. But you do it because it is right, even when it costs you something, even when it is unpopular.
"France and Rwanda are going to relate much better to the benefit of both our peoples, economically, politically and in terms of culture.
"But the relationship between our two countries will never be entirely conventional. There is a special familiarity resulting from the complex and terrible history we share."
Macron made the speech as he began a highly symbolic two-country African tour. The tone of his comments closely reflected the conclusions of an independent report released in April that he commissioned.
That report concluded that France bore "heavy and overwhelming" responsibility for not doing more to stop the genocide, but that it was not complicit in the slaughter.
Shortly afterwards Rwanda released a report that found France was aware a genocide was being prepared and bore responsibility for enabling it by continuing support for Juvenal Habyarimana, Rwanda's president at the time.