The Argentinian pontiff, who has often strongly defended indigenous rights since his election in 2013, made his comments on protection of native lands to representative of tribes attending the Indigenous Peoples Forum in Rome.
While he did not name the pipeline, he used strong and clear language applicable to the conflict, saying development had to be reconciled with “the protection of the particular characteristics of indigenous peoples and their territories”.
His comments came within days of a US federal judge denying a request by tribes to halt construction of the final link of the project that sparked months of protests by activists aimed at stopping the 1,170-mile line.
The tribe and its supporters believe the pipeline poses a threat to a reservoir that supplies the tribe's drinking water. The pipeline project, which crosses four states, is estimated to be able to transport 570,000 barrels of oil a day.
Speaking in Spanish, Pope Francis said the need to protect native territories was “especially clear when planning economic activities which may interfere with indigenous cultures and their ancestral relationship to the earth”.
The Standing Rock Sioux and Cheyenne River Sioux tribes have argued the project would prevent them from practising religious ceremonies at a lake they say is surrounded by sacred ground.
“In this regard, the right to prior and informed consent (of native peoples) should always prevail,” the pope said, citing the 1997 UN Declaration on the Rights of Indigenous Peoples.
Thousands of tribe members, environmentalists and others set up camps last year on Army Corps land in the North Dakota plains as protests intensified.
In December, the administration of former US President Barack Obama denied the last permit needed by Energy Transfer Partners, which is building the $3.8 billion (£3.05 billion) pipeline.
But last week, the US Army Corps of Engineers granted a final easement, after President Donald Trump issued an order to advance the project days after he took office in January.
The pope made an indirect criticism last week of another Trump project, a wall along the border with Mexico, saying society should not create “walls but bridges” and ask others to pay for them.
Pope Francis, who wrote a major encyclical letter in 2015 on climate change and the environment, told the group that new technologies could be legitimate but had to respect the earth.
“Do not allow those which destroy the earth, which destroy the environment and the ecological balance, and which end up destroying the wisdom of peoples,” he said.
Join our new commenting forum
Join thought-provoking conversations, follow other Independent readers and see their replies