The papacy has not always had a good time at the Venice Biennale. In 1999, most strikingly, visitors were treated to the sight of a lifesize wax image of Pope John Paul II being struck down by a meteorite, courtesy of the artist Maurizio Cattelan.
This year, though, the Vatican has chosen to enter the first ever Pavilion of the Holy See, becoming one of the 88 nations to show work at this cacophonous, often irreligious festival of art from across the world.
The Holy See pavilion takes the first 11 books of Genesis as its starting point. Its title – Creation, Uncreation, Re-creation – hints at ideas "fundamental for culture and for church tradition", according to Cardinal Gianfranco Ravasi, the president of the pontifical council for culture and the figure behind the Holy See's appearance at the biennale.
Three rooms of works take on the themes in turn: interactive videos by the Milanese collective Studio Azzurro focus on creation; then come stark images of man's destructiveness by Czech photographer Josef Koudelka. Paintings hinting at hope and renewal by American Lawrence Carroll complete the all-male lineup.
Reactions to the the pavilion have already been mixed – from admiration at the Vatican's willingness to engage with the art world to disappointment that the Holy See, historically the most important patron of art in the western world, has fielded what in some quarters is regarded as a kind of all-purpose spiritual mishmash.
The author of Fides et Forma, an Italian blog on art, architecture and the Catholic church, has written that the money for the pavilion (albeit privately raised) was being "spent on an absurd event" and "an insignificant mental rumination by a few individuals".
Staging the exhibition was "an act of egotism, not of love for the church and Jesus". Under the headline "A 'diabolical' Biennale", the blogger also expressed concerns that the huge main biennale exhibition – one of whose major themes is mysticism, magic and alternative belief systems – is showing tarot cards designed by the English occultist Aleister Crowley.
But according to the curator of the pavilion, Micol Forti, who is also the curator of 19th-century and contemporary art in the the Vatican museums, involvement in the biennale is an opportunity for the Roman Catholic church.
"It's very important for the Holy See to be here: it's a different situation where you can create a space for a dialogue with different ideas, different ideological thinking, different religions," she said. "Here at the biennale, it is not important where you are from: the only important thing is that there is a place where you can speak."
They had deliberately steered clear of work that engaged directly with Catholic themes or imagery, she said. "For Cardinal Ravasi, it is very important to distinguish between religious and liturgical artwork and that which engages with spiritual ideas. The Sistine chapel is a church: it contains completely revolutionary artworks but it is still a church.
"[The Holy See pavilion] is not a church; this is a completely different context. We respect this context: it is a place for international art from different contexts, philosophies, culture and religions."
Forti said that she and the selection committee for the pavilion "never asked the artists whether they believed or not. We started from the topic of the exhibition: for me it was important that there was intellectual honesty, a clear path in the artists' thinking."
As he made the final touches to his room of paintings, Carroll, who is based near Rome, said: "I have an Irish mother, and I was raised a Catholic, but whether we were members of the church or not was never a question asked of any of the artists. It was not important whether we were atheists, Jewish or Catholic."
He added: "I applaud Cardinal Ravasi for this – it was very difficult and controversial within the church because many people don't want this kind of dialogue. But how beautiful to invite atheists, anyone, into a dialogue."
He said there had been no guidance or censorship from the Holy See: "I made my work in the way that I always do."
He had no hesitation in accepting the invitation to represent the Holy See. "You can look at any national pavilion and ask whether an artist would want to show with them," he said. "If you look at America, you can think about the wars they have been involved in, the drones … What's more important is the bridge they are trying to create – the idea of a bridge and the extension of a hand."
"It's very important that the church was to have a relationship with the culture outside: it's a first step towards both speaking and listening," said Forti.
• The Venice Biennale runs from 1 June to 24 November