The film has fuelled disagreements over whether Pope Joan really existed or, as the Church has always maintained, she was a mythical figure used by the early Protestant Church to discredit and embarrass Rome.
For a Church that even in the 21st century remains staunchly opposed to the idea of female priests, a female Pope was anathema.
To make matters worse, the deception is said to only have been found out when Joan gave birth during a procession through the streets of Rome.
The medieval epic stars a German actress, Johanna Wokalek, as the female Pope, the American actor John Goodman as Pope Sergius and David Wenham, an Australian last seen in the Lord of the Rings trilogy, as her lover, a knight named Gerold.
It is based on a highly contentious story – that in the ninth century, a baby girl was born in Germany to English parents, who had moved to the Continent as Christian missionaries.
According to the legend, she grew up to be an unusually intelligent young girl and, frustrated by a lack of opportunity for women, disguised herself as a boy in order to enter a Benedictine monastery, calling herself Brother John Anglicus.
She studied for a while in Greece before arriving in Rome, where she so impressed the Vatican with her abilities that she became a cardinal and was eventually elected pontiff in 853, after the death of Pope Leo IV.
She supposedly ruled as head of the Church for nearly three years, before her deception was found out.
One improbable account insists that she was riding a horse near the Colosseum when she suddenly went into labour.
The crowd, shocked and angered to find that the Holy Father was in fact a holy mother, either stoned her to death or tied her to the horse and had her dragged through the streets of Rome.
The Catholic Church has long argued that Pope Joan is not mentioned in any contemporary records and that the whole tale is a fantasy, cooked up by scheming Protestants.
L'Avvenire, the newspaper of the Italian Bishops' Conference, last week dismissed the movie as "a hoax" and a film of "extremely limited vision".
But proponents of the story point out that papal records are almost non-existent in the 10th and 11th centuries and that even male popes are barely documented.
They point to one particularly extraordinary artefact as evidence that she existed – a wooden chair with a hole in the seat which, it is claimed, was used for 600 years to establish the gender of would-be popes in the wake of the Pope Joan scandal.
Papal candidates were supposedly made to sit on the 'sella stercoraria', which is today owned by the Vatican Museums, while a deacon prodded their genitalia from underneath to make sure of their manhood.
"Joan's absence from contemporary church records is only to be expected. The Roman clergymen of the day, appalled by the great deception visited upon them, would have gone to great lengths to bury all written reports of the embarrassing episode," argues the American writer Donna Woolfolk Cross, on whose novel, 'Pope Joan', the film is based.
"The Dark Ages really were the dark ages," said Peter Stanford, a former editor of the Catholic Herald and the author of 'The She-Pope: a quest for the truth behind the mystery of Pope Joan'.
"There is absolutely no certainty about who the popes of the ninth century were. We have to rely instead on medieval chronicles, written hundreds of years later.
"It's perfectly feasible that Joan existed. A monk's cowl is baggy and well suited to covering up a woman's body. We know that some women bound their breasts and cut their hair to pass themselves off as men." He dismisses the Catholic line that the story of Pope Joan was the product of Protestant black propaganda.
"That is categorically not true. There are plenty of pre-Reformation Catholic texts which mention Pope Joan. They were written by bishops, archbishops – even a secretary to a pope. They all accept that she existed. The Catholic Church was embarrassed by the story and just erased it from the records, sometimes very crudely."
Official histories of the popes make no mention of Pope Joan and many historians dismiss the story as a fable.
The truth about her may never be known, but the story continues to fascinate modern audiences.
The film reached the top 10 of most popular movies in Italian cinemas last week, just behind Hollywood blockbusters such as Robin Hood and Sex and the City 2.
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