Old St. Peter's Basilica

Construction began by order of the emperor Constantine I on the slope of the Vatican Hill, over a necropolis at the edge of the Circus of Nero. The spot had been marked since at least the second century as the grave of Saint Peter, and Constantine and Pope Sylvester I built on the place they believed held it: the mausolea were cut down, the burial chambers filled in and the ground levelled into a platform, the platea Sancti Petri. Levelling a cemetery still in use was unusual in religious and legal terms alike, justified by Christians on the authenticity attributed to the apostle's burial. The work is placed in the 320s; how long it ran is not agreed, one account allowing about forty years, another the church substantially finished by 333.

Since the site lay outside the ancient city, the apse and altar were set at the west end so that the façade was approached from Rome to the east. Five aisles divided by colonnades of marble columns taken from earlier pagan buildings held 3,000 to 4,000 worshippers under a timbered roof. Around the apostle's shrine stood a screen of twisted columns which tradition said Constantine had taken from the Temple of Solomon, though they probably came from an Eastern church.

When the Ostrogothic king Totila took Rome on 17 December 546, Roman senators and patricians sheltered in the basilica. Papal coronations were held there, and in 800 Charlemagne was crowned emperor; Charles the Bald, the three Ottos, Frederick Barbarossa and Frederick II were among those crowned after him. Saracen raiders sacked the church in 846. Some basilicas, St Peter's among them, stood outside the Aurelian Walls and were easy targets, "filled to overflowing with rich liturgical vessels and with jeweled reliquaries". The raiders destroyed Saint Peter's tomb, pillaged the shrine and carried off furnishings including the seventh-century bronze doors. Pope Leo IV rebuilt the damaged parts and enclosed the whole area in the Leonine wall.

Cardinal Jacopo Stefaneschi commissioned the Navicella mosaic, attributed to Giotto and dated 1305–1313, for the wall above the entrance arcade; it showed Peter walking on the water, a seascape of a kind known only from ancient art. Stefaneschi also commissioned the triptych Giotto signed for one of the church's altars.

The papacy, which had lived beside the Lateran, moved to the Vatican only after Avignon, from 1377. By the fifteenth century the church was falling into ruin, the roof decayed and the north wall leaning out of true. Nicholas V resolved on a thorough renewal; Leon Battista Alberti was consulted and Bernardo Rossellino given the work, which improved the apse but was long interrupted. Alberti pronounced the building a structural abomination: "an extremely long and high wall has been constructed over a continuous series of openings, with no curves to give it strength, and no buttresses to lend it support", the wind having already displaced it more than six feet from the vertical. In the 1490s Antonio del Pollaiuolo made bronze tomb effigies for Innocent VIII and Sixtus IV.

Julius II at first intended to preserve the old building, then turned to tearing it down and building anew. Many were shocked by the proposal, the basilica standing for papal continuity going back to Saint Peter; the original altar was to be kept in the new structure. Demolition began at the presbytery and went on for a century. Part of the Constantinian nave, walled off from the new crossing under Paul III, stayed in use for most of the works; accounts differ on when the last of it came down: in 1605, or in 1609 under Paul V, against renewed objections.

Most of the tombs were destroyed in the demolitions of the sixteenth and seventeenth centuries; bones were still being turned up in February 1544. Sarcophagi and their contents were moved to the new basilica and a handful of other Roman churches, but only Pollaiuolo's two papal tombs were properly reconstructed there. With the translations from the catacombs and two fourteenth-century fires at St John Lateran, the rebuilding is held responsible for the destruction of about half of all papal tombs, and Donato Bramante, chief architect of the new church, has been remembered as Maestro Ruinante. The Navicella was largely destroyed, though fragments were preserved, and devotion to the old basilica moved Tiberio Alfarano, Onofrio Panvinio and Giacomo Grimaldi to set down minute descriptions of what was being lost before the new basilica was consecrated in 1626.