He said the church had not imposed itself on the indigenous peoples of the Americas.
Since Colombus's landing, millions of tribal Indians are believed to have died as a result of European colonisation backed by the Roman Catholic church through murder, disease or enslavement.
Many Indians today struggle for survival, stripped of their traditional ways of life and excluded from society.
"To say the cultural decimation of our people represents a purification is offensive, and frankly, frightening"
Sandro Tuxa, leader of the movement of northeastern tribes
Indian groups sent a letter to Benedict last week asking for support in defending their ancestral lands and culture.
The letter said the Indians had suffered a "process of genocide" since the first European colonisers had arrived.
Priests blessed conquistadors as they waged war on tribal Indians.
Other tribal leaders also voiced their criticism on Monday.
Dionito Jose de Souza, a leader of the Makuxi tribe in northern Roraima state, said: "The state used the church to do the dirty work in colonising the Indians but they already asked forgiveness for that ... so is the pope taking back the church's word?"
Pope John Paul II spoke in 1992 of mistakes in the evangelisation of native peoples of the Americas.
"We repudiate the [pope's] comments," said Sandro Tuxa, leader of the movement of northeastern tribes.
"To say the cultural decimation of our people represents a purification is offensive, and frankly, frightening.
"I think [the pope] has been poorly advised."
The Roman Catholic church's own Indian advocacy group in Brazil also criticised Benedict's speech.
Paulo Suess, the advocacy group's adviser, said: "The pope doesn't understand the reality of the Indians here, his statement was wrong and indefensible."