Andy Burnham is becoming the country's first openly Catholic PM – nearly 500 years after Henry VIII split from Rome.
The longstanding religious divide means that measures are in place to protect the Church of England.
Under a law from the 19th century, Mr Burnham will be barred from advising the King on top appointments to the Church.
The Roman Catholic Relief Act of 1829 states that anyone breaking this law shall be 'deemed guilty of a high misdemeanour, and disabled for ever from holding any office'.
However, in practice Mr Burnham will simply delegate those duties to another Government minister.
Under a law from the 19th century, as a Catholic Andy Burnham is barred from advising the King on top appointments to the Church of England
Henry VII split from Rome five centuries ago, with the religious divide defining the country's history
Mr Burnham, who was born in Merseyside, inherited his faith from his mother and attended Catholic schools.
The constitutional conundrum was previously raised when Boris Johnson was prime minister.
Mr Johnson is widely accepted to have been Britain's first Catholic premier, despite him having technically entered Downing Street in 2019 as an Anglican.
Sir Tony Blair also converted to Catholicism within months of leaving No10.
Richard Moth, the Archbishop of Westminster and leader of the Catholic Church in England and Wales, previously suggested Mr Burnham would draw on his faith in office.
'It certainly has meaning to me, and I'm sure it does to him,' he said.
'As a Catholic, a Christian, one thinks out of that space, if you like, and that informs conscience, it informs the way we think about things.'
The Archbishop of Westminster told the BBC: 'Certainly, looking at it from a Catholic perspective... [there is] a really big accent on the value of the human person.
'And I really do hope that we're going to see that real concern for humanity, not just in the grand scale, but... the needs of families, the needs of the homeless, all that will come from his Catholic understanding, I think.'
Mr Burnham has been open about his Catholic faith in the past, telling The Guardian in 2009 that the three most important things in his life, aside from family, are 'Everton FC, the Labour Party and the Catholic church - in that order'.
But the strength of his faith appeared to have fluctuated in 2015, when he told the Huffington Post website: 'I'm Catholic by upbringing, but I'm not particularly religious now.'
The father-of-three added: 'My kids go to a Catholic school, so I still believe in the values and the grounding it gives you, I'm a very big believer in that.'
Archbishop of Canterbury Dame Sarah Mullally, the most senior bishop in the Church of England
In the same interview, Mr Burnham suggested the Catholic Church had lost touch with millions of ordinary British Catholics on issues like gay rights and birth control.
'I find that quite difficult because if I think of the church of my youth, and the priests that I knew, the feeling and overriding mood was quite forgiving really, quite humane, humorous, irreverent, even the priests,' he said.
'That's my memory of the church that I grew up with. And it seemed at some point... to click into a more judgmental mode and became much more obsessed with sexuality and issues related to sexual behaviour.'
But Mr Burnham stressed he still values his Catholic upbringing, adding: 'Catholic social teaching underpins my politics'.