The church is named after St Ouen (or Audoen) of Rouen (Normandy), a saint who lived in the seventh century and was dedicated to him by the Anglo-Normans, who arrived in Dublin after 1172.

In 1485 Sir Roland Fitz-Eustace, Baron Portlester, erected a new chapel next to the nave, in gratitude for his preservation from a shipwreck near the site.

[3] Strenuous efforts were made over the next few years to repair the roof, steeple and pillars of the building, and the guild was ordered to contribute its share.

In 1671 Michael Boyle, the Church of Ireland Primate, ordered the "annoyance of the buttermilke market" under St Audoen's to be closed.

[5] St Anne's Guild, which had managed to secret away its extensive properties after the Reformation, and which had remained under Roman Catholic control, never did give up its holdings, despite several investigations and court orders lasting until 1702.

St Audoen's parish was once the wealthiest within the city and the church was for hundreds of years frequented on State occasions by the Lord Mayor and Corporation.

[8] In July 1536 George Browne arrived in Ireland as Archbishop of Dublin, and a few years later he energetically pushed through the wishes of Henry VIII to be recognized as supreme head of the Irish church.

In 1547 the assets of the parish were appropriated by the state church that was established following the English Reformation (more particularly the Tudor conquest of Ireland).

A few years later St Anne's chapel, which had lost its roof and many monuments, was re-roofed and converted to a visitor reception centre, which included an exhibition on the history of the church.

In 1826 it disappeared for twenty years, until found in front of the newly erected Catholic Church in High Street.

[4] In the porch of the western door lie the fifteenth-century monuments of Sir Roland Fitz-Eustace, Lord Portlester, who died in 1496, and his third wife, Margaret (née D'Artois).

[20] In the North Nave is a memorial, with Corinthian columns and a pediment, to Sir William Sparke (died 1623), one of the justices of the Court of King's Bench (Ireland), erected by his widow Mary Bryce.

Many notables were buried there, including many bishops and Lord Mayors of the city and the families of Ball, Bath, Blakeney, Browne, Cusack, Desminier, Fagan, Foster, Fyan, Gifford, Gilbert, Malone, Mapas, Molesworth, Penteny, Perceval, Quinn, Talbot and Ussher.

[28] The Curate-assistant Christopher Teeling McCready (1836–1913)[29] collected detailed genealogies of some of these families in seven hand-written volumes, which are now in Marsh's Library.

Among the burials within the church and graveyard are: On 11 March 1597, a massive accidental gunpowder explosion in one of the nearby quays damaged the tower of St. Audoen's.

In the 1640s, at the time of the Catholic Confederate Rebellion, the burghers of the city could see from the church tower the fires of their opponents burning in the distance.

In 1733 a popular Alderman, Humphrey Frend, was returned at an election by a large majority, and two barrels of pitch were burned as a celebration at the top of St. Audoen's tower.

[31] In 1793 a petition was sent from the vestry, requesting the removal of the police on the grounds of expense and inefficiency, and for the return of the night watchman originally appointed by the parish.

[4] St Audoen's Church houses a fine organ built in 1885 by the firm Forster and Andrews, of Hull.