'I won't forget what you said, ' he told the pope after their meeting. "We had a fantastic meeting". "That's all he wanted", adding it should "very much" be seen as a slight.
Francis's interpreter could be heard translating a comment by the pope to the first lady: "What do you give him to eat?"
Trump has never been one to let an insult, perceived or real, go by without a response, and he made no exception for the world's best-known religious leader. Trump was expected to be given a tour of the Vatican after he arrived and then meet with the pontiff in his library.
The US president was greeted by Archbishop Georg Ganswein, the head of the papal household, and escorted by the Swiss Guard to the offices of Pope Francis.
"The @Potus and I are looking forward to our visit with His Holiness Pope Francis @Pontifex". The meeting appeared quite respectful but the Pope left Trump with an epic gift: the encyclical he penned on climate change.
A statement from the Vatican said that "satisfaction was expressed" at their "joint commitment in favor of life" and that there was hoped-for collaboration on health care, assistance to immigrants and protection of Christian communities in the Middle East.
On global affairs, their "exchange of views" covered the "promotion of peace in the world through political negotiation and interreligious dialogue", and highlighted the need to protect Christian communities in the Middle East.
The two men spoke privately for about 20 minutes before joining the rest of the entourage and posing for photographs.
Trump gave Francis a boxed set of five first-edition books by Martin Luther King Jr. and a bronze sculpture titled "Rising Above", representing a peaceful tomorrow and created to evoke the values of unity and resilience.
It is a clear message for Americans watching from home, most of all: Their leaders will pay homage to backward Catholic traditions.
Asked by European Commission President Jean-Claude Juncker as they began talks in front of a battery of cameras if he was exhausted, Trump, 70, said he had "covered a lot of countries, lot of leaders, some great leaders". The pontiff was then introduced to members of Trump's delegation, including his wife Melania, his daughter Ivanka and son-in-law Jared Kushner, as well as aides Hope Hicks and Dan Scavino.
Melania, a Catholic, asked the Pope to bless her rosary beads. "Potica?" - a reference to a calorie-laden cake from Slovenia, her country of birth. She laughed in response, and agreed with him.
He later flew to Brussels where he was to meet Belgium's king and prime minister on Wednesday evening before a day of meetings with European Union and North Atlantic Treaty Organisation leaders on Thursday.