Red-hatted cardinals, bishops, candle-carrying friars and helmeted Swiss Guards walked slowly into the vast, sunlit square in front of the basilica as a choir chanted psalms and prayers in Latin while a bell gently tolled, as he was taken from the Vatican hotel where he live to the basilica.
The body of the 88-year-old pontiff, who died two days ago in his rooms at the Santa Marta guesthouse after suffering a stroke, was held aloft on a wooden platform by 14 white-gloved, black-suited pallbearers.
As the coffin crossed St Peter's Square, a crowd of several thousand broke into repeated applause - a traditional Italian sign of respect at such events.
Francis, who had only recently left hospital after five weeks being treated for double pneumonia, last appeared in public on Sunday, when he delighted onlookers gathered to celebrate Easter by being driven around the packed square in his white, open-topped popemobile.
Vatican officials rushed on Wednesday to help the pallbearers carry the coffin up a stone incline, before the procession passed through St Peter's giant bronze doors and into the hushed interior of the ornate, cavernous church.
Francis' body will lie in state in St Peter's Basilica until Friday evening, allowing the faithful to pay their respects.
His funeral is set for Saturday and will draw heads of state and government from around the world, including US President Donald Trump, who clashed repeatedly with the pope on social issues such as immigration.
Leaders from Italy, France, Germany, Britain, Ukraine, Brazil, EU institutions and Francis' home nation of Argentina have also confirmed their presence, among many others.
A conclave to choose the new pope is not expected to start before May 6.
The cardinals gathering in Rome will decide the date following what are often prolonged discussions.
There is no clear frontrunner to succeed Francis, who was from Argentina and was the first non-European pope in 1300 years, although British bookmakers have singled out Luis Antonio Tagle, a reformer from the Philippines, and Pietro Parolin, from Italy, as early favourites.
Tagle and Parolin stood together in the basilica, flanked by about 80 other cardinals, as the wooden coffin was laid on a dais in front of the altar, built on the spot where St Peter, the first pope, is believed to have been buried after dying as a martyr in the reign of Emperor Nero (AD54-68).
Francis's body was dressed in red vestments, his hands clasped together holding a rosary, and a white mitre on his head.
Cardinal Raymond Burke, a US-born conservative prelate who was often at odds with Francis during his 12-year papacy, was among those who approached the coffin and bowed.
Francis shunned much of the great pomp and ceremony traditionally associated with the role of head of the world's 1.4 billion Roman Catholics.
He clashed repeatedly with traditionalists, who saw him as overly liberal and too accommodating to minority groups, such as the LGBTQI community.
In electing a new pope, cardinals will have to consider whether to complete Francis' promised reform of the Church, making more room for women in senior positions and being more amenable to an evolving society, or opt for retrenchment.
Some 135 cardinals are eligible to take part in the secretive conclave, which can stretch over days before white smoke pouring from the chimney of the Sistine Chapel tells the world that a new pope has been picked.