The pontiff, with Michelangelo's celebrated frescos above and behind him, was baptising 33 infants, when he told the mothers present that it was alright to feed their children.
"Mothers, give your children milk if they cry because they are hungry; breastfeed them. And you can do even now, don't worry," he said, in a change to his prepared homily.
Instead of using the term "give them milk", he used "allattateli", which in Italian means "breastfeed them", and he added that they should not hesitate.
Francis even said a prayer for those mothers who had problems breastfeeding.
"We thank the Lord for the women with milk and we pray for those who are not able to breastfeed their babies. We pray for them and try to help them," he said.
The consternation aroused in some by breastfeeding in public was underlined last month when a mother was asked to cover herself in the tearoom of the luxury London hotel Claridge's in Mayfair, after attempting to breastfeed her child.
Claridge's said later it "embraces" breastfeeding but asks that women are "discreet towards other guests".
But a group of 40 mothers staged a mass "nurse-in" outside the hotel.
Back in 2007, there were protests in Madrid after a mother was asked to leave the Prado art gallery after she began breastfeeding.
Sunday's comments by the Pope were not the first instance of his taking an accommodating line on babies in church.
Last month, during a visit to the St Joseph church in Rome, the Pope called on parishioners to be more tolerant of infants. "Babies cry; they make a noise," he said.
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