That investment has since been the subject of a financial investigation.
Resignations at this level of the Vatican are extremely rare and the Holy See said little in its communique released late on Thursday.
“The Holy Father accepted the resignation from the office of Prefect of the Congregation for the Causes of Saints and from the rights connected to the Cardinalate, presented by His Eminence Cardinal Giovanni Angelo Becciu,” a statement said.
But the cardinal, 72, told Italian website Domani he was being forced to resign because he was suspected of gifting Church money to his brothers.
“I didn’t steal even one euro. I am not under investigation but if they send me to trial, I will defend myself,” he said.
Relaying the turnout of events later at a news conference, the cardinal said his removal had come “like a bolt out of the blue”. He said the Pope “was suffering” when he delivered the news.
“It’s all surreal. Up until yesterday… I felt I was a friend of the Pope, the faithful executor of the Pope.
“Then the Pope told me that he no longer had faith in me because he got a report from magistrates that I committed an act of misappropriation.”
Cardinal Becciu reconfirmed that there had been “a misunderstanding”, adding: “I am ready to explain everything to the Pope. I have not done anything wrong.”
“I said to the Pope: why are you doing this to me, in front of the whole world?”
The anguished words of one of the Church’s most senior cardinals – now fired and stripped of his right to choose the next Pope.
Giovanni Angelo Becciu had functioned as Deputy Secretary of State – a role with unrestrained access to Pope Francis – and was latterly head of the department that selects future saints.
However, on Thursday evening, he was called upon by his Boss for a reportedly tense meeting with his boss. Cardinal Becciu had managed a controversial €200m (£180m) purchase of a London property with Church funds, including alms money. Other reports allege he propped up a failing Roman hospital which employed his niece.
“The Holy Father explained that I had given favours to my brothers and their businesses with Church money… but I am certain there are no crimes”, he told new Italian newspaper Domani.
But his denial couldn’t salvage the situation. It’s been tagged an “earthquake at the Vatican”.
The turn out of events of his dismissal may seem cloak-and-dagger – but it is a reminder yet again that the scandal and corruption that beset governments across the world also reach the highest echelons of the Holy See.