Herbert de Losinga, Bishop of Norwich, founded the church in 1095 to serve a Benedictine priory subordinate to the Priory of the Holy Trinity in Norwich. He dedicated it to Margaret of Antioch, the early-Christian martyr whose iconography - emerging from a dragon - made her one of the most popular saints in medieval England. The original Norman building has almost vanished, but its base survives at the foot of the south-west tower, an Early English Gothic structure of the 12th century that still leans noticeably westward. The larger north-west tower came later, in the Perpendicular style of the 15th century, and the chancel with its clerestory dates from the 13th century. The towers face the Saturday Market Place that Herbert de Losinga also founded, completing the medieval staging set that became the heart of King's Lynn.

St Margaret's was the parish church Margery Kempe knew - the mystic and pilgrim who, around 1438, dictated The Book of Margery Kempe in nearby Bishop's Lynn and produced what is widely considered the first autobiography in English. Margery wept loudly in this nave, often in front of the rood, often to the irritation of fellow worshippers. She heard sermons here, debated her visions with priests here, and set out from this church on her pilgrimages to Jerusalem, Rome, Compostela, and Norway. The book was lost for centuries and rediscovered only in 1934 in a Lancashire country house. The space where its strangest, most operatic episodes unfolded survives intact, with the 13th-century chancel and clerestory still rising above the spot where Margery once knelt and 'cryed wonder lowde.'

By 1741, the central lantern tower and the south-west spire had become structurally exhausted. They fell during a winter storm, taking much of the nave with them. Matthew Brettingham, who would later work as a draughtsman on Holkham Hall, was hired to rebuild. Between 1745 and 1746 he raised a new nave in a style that historians now recognise as early Gothic revival - lighter than the medieval original, with pointed arches confidently abstracted rather than slavishly copied. The bells in the tower were recast in the same period; five of the current ten date from that mid-18th-century campaign. The organ, by John Snetzler, also arrived in the 1750s. The latest of many restorations was completed by Holmes and Swift in 2003, and the instrument is recorded in detail on the National Pipe Organ Register.

After the English Reformation, St Margaret's became the parish church for the town of King's Lynn. Its endowment was reassigned to Norwich Cathedral, and the last prior, Drake, was given the fourth stall in Norwich as a prebend. In 2011, the church received a new title: King's Lynn Minster, the elevated designation given to historically significant churches that serve a wider community than a single parish. The grade I listed building still stands on the south side of the Saturday Market Place, its mismatched towers presiding over what was once medieval England's most important port. Step inside and the geometry is honest about its history - 12th-century stone at the base of one tower, 15th-century perpendicular tracery in the other, an 18th-century Gothic nave between them, and a 13th-century chancel rising above the altar. The architecture admits, generously, that no single century built it.