The Argentine has refused the traditional trappings of the papacy from the start, declining to move into the sumptuous papal apartment in the Vatican and plumping instead to live in a hotel inside the tiny city state.
Francis's decision will allow visitors access to the bedroom where more than 15 popes have slept over the centuries, furnished with a gilded bed and two bedside tables in wood and marble.
The bed has also served another purpose — during the Second World War, when the 55-hectare (135-acre) residence was opened to refugees, some 40 children were born there.
“Here, the grand events of history mix with personal histories,” said Osvaldo Gianoli, director of the pontifical villas.
“The opening of the private apartments has a symbolic value which reflects the pastoral beliefs of Pope Francis,” Gianoli said during an inauguration ceremony on Friday.
The second-floor apartments still bear the traces of the frequent visits of Francis's predecessor, Benedict XVI — for example 12 volumes of a German theological lexicon line the shelves of the study.
The German came to this hilltop palace, with its view over lake Albano, after his shock announcement in 2013 that he would become the first pontiff in seven centuries to resign from the role.
Saverio Petrillo — who spent 56 years in service to seven popes at the residence — recalled how John XXIII (1958-1963) would slip out without an escort and drive to neighbouring castles, on one occasion almost missing prayers.
Francis opened the estate's gardens to the public in 2014, with tours organised for groups and by reservation only.
Since last year, tourists have also been able to climb aboard a special white train for an express trip to the lavish estate and a tour of the papal villa, including past the pope's organic farm, which includes cows, free-range hens, cockerels and pontifical bees.
Francis's absence from the palace is not exceptional — of the 33 popes who could have stayed there only around half have done so, according to Antonio Palucci, director of the Vatican museums. His successors will be able to return there if they wish.