The announcement that the Vatican will be a major player at next year's Venice Biennale marks the return of the Church as a patron of contemporary art, something it is uniquely able to do as long as it eschews the fads and foibles of today's marketplace

At the 2005 Venice Biennale, the Church of San Lio hosted a small exhibition of contemporary religious art sponsored by the National Department for Ecclesiastical Cultural Heritage of the Italian Episcopal Conference. None of the Italian artists participating was internationally famous, and the event went unrecorded in the world's press. Three years on and the Catholic Church is rolling out the big guns. Archbishop Gianfranco Ravasi, president of the Pontifical Council for Culture, announced last month that the Vatican will have its own pavilion at the fifty-third International Art Exhibition next year.

This is a long way from 1954, when L'Osservatore Romano denounced the Biennale as a symptom of "the breakdown of art in modern times". Now we have Archbishop Ravasi telling the press: "Venice is a showcase for all the big countries in the world and the Holy See would like to be there too. We're trying to get the best of international artists on our side who can create new works with a religious or spiritual subject".

Actually, this is not a bolt from the blue. There has long been a feeling abroad in the Holy See that the Church, once the greatest sponsor of art in Europe, should make its peace with contemporary practitioners. Indeed, the first move towards acceptance was made as early as 1947 when Pius XII's encyclical Mediator Dei acknowledged that sacred art, while remaining reverential, should "still reflect the spirit of our time". In the 1960s, the modern-art-loving Paul VI went further, reinstating the Vatican tradition of art collecting; since his reign, more than 500 contemporary works have entered the Vatican Museum.

But the present discussion is not about art in museums; it's about art in churches. With the Vatican also planning participation in this autumn's Venice Biennale of Architecture, it appears to be announcing a new post-modern era of church patronage, in which cutting-edge ecclesiastical buildings such as Renzo Piano's Padre Pio Pilgrimage Church in Foggia will be filled with equally cutting-edge art. If so, it's a welcome change of direction after a century of half-baked modernism that must surely mark the nadir of ecclesiastical art. The only question is, why suddenly now? Maybe the Vatican is tired of hearing art galleries hailed as the new churches and gallery-going as the new form of Sunday worship, and feels that it's time to snatch the initiative back.

In the field of architecture, the global race is on to build ever grander temples to the arts, with Abu Dhabi currently out in front after commissioning a constellation of architecture stars to turn Saadiyat Island into a place of cultural pilgrimage. The Vatican may quite reasonably be wondering why the Devil should have all the best buildings. But what applies in architecture doesn't necessarily apply in art. The services of the world's most prominent architects are essential for the realisation of large-scale projects, which only they have the resources to tackle. But great art can be created by unknown artists in a space no bigger than Van Gogh's bedroom. So when Archbishop Ravasi says, "We are looking for world-famous people," you have to ask why.

The Church has reason to feel cheated in the contemporary art stakes when several leading artists have based their success on the exploitation of Christian imagery. In Britain, Damien Hirst has made a killing out of Catholic iconography and the Chapman Brothers are doing nicely too, with their latest vision of hell on show at the White Cube gallery in St James's, London, and their contemporary take on the Book of Revelations to be revealed later this year. Theirs are not names, thankfully, on the Vatican's wish list, said to include Anish Kapoor and Bill Viola - artists who make meditative works conducive to spiritual contemplation.

Still, the emphasis on world fame is a little worrying, suggesting that the Vatican, after years of sitting on the sidelines watching artists achieve fame on the back of Christianity, feels its turn has come to hitch a ride on their coat-tails. Either that, or it believes that by siting works by world-famous artists in churches, it will pull in the Sunday gallery-going crowd. But if that crowd is attracted by fame, it will move on to a different venue the Sunday after.

The Church does not need to court fame; it is famous enough. Nor does it need to worry about achieving returns on its art investments. Unlike public galleries, the pontifical committee tasked with selecting artists needn't justify its choices on financial grounds; it can apply an alternative scale of spiritual values. It is in the privileged and enviable position of being able to ignore the art-world tipsters, and to back outsiders. So instead of dipping a toe in the shallow end of superficial reputation, it should give itself time to explore the depths. It should also cast its net wide. As St Martin-in-the-Fields proved with two recent works commissioned from non-Christian artists - a crib from Japan's Tomoaki Suzuki and a window from the Iran-born Shirazeh Houshiary - outsiders can bring a new spiritual energy to familiar genres.

There is also a distinction to be made between art on spiritual subjects and spiritual art. As White Cube's exhibitions director, Tim Marlow, pointed out in last week's Independent on Sunday, contemporary artists who use religious iconography often do it "in a critical and questioning manner". He wondered, with reason, "whether the Church can commission work that is both provocative and questioning". Yet if the Church excludes the provocative and questioning, it will find its pool of famous artists very small. In our media-led society, artists who question and provoke rise to greater prominence than quiet seekers after spiritual truth.

Prominence, moreover, comes at a price. Aware of this, the Vatican has let it be known that it is seeking wealthy patrons to sponsor artworks for churches. This is a strategy that could lead it into murky waters. The art world has changed a lot since the Renaissance. The great art patrons of the past who paid for the construction and decoration of Catholic churches may have gained in personal glory, but not in wealth. These days, however, a patron who sponsors an artwork for display in a church gains access to a prestigious showcase that can enhance the artist's stature and market value. If the patron collected or dealt in the artist's work, the Church could become a pawn in an art-market game.

But there's a better reason why the Vatican should forget fame, follow its spiritual instincts and take its search for artists out to the highways and hedges. With the galloping commercialisation of contemporary art, there's a crying need for independent patrons who take the long view and are not in the market to make a quick buck. The Church could be just such a patron, championing the cause of a spiritual, slow-burning art, an art designed not for provocation or instant gratification but for contemplation - an art, like the great church art of the past, made to last.

The Church's new dialogue with contemporary art could be a marriage made in heaven. But marriages made in a hurry - or for the sake of fame - don't last. Fortunately, in our fast-paced world, the Church is one institution that can take its time.