The St Albans area has a long history of settlement. The Celtic Catuvellauni tribe had a settlement at Prae Hill a mile or so to the west. The Roman town of Verulamium, second-largest town in Roman Britain after Londinium, was built alongside this in the valley of the River Ver a little nearer to the present town centre.

After the Roman withdrawal, and prior to becoming known as St Albans, the town was called Verlamchester or Węclingacaester by the Mercian Angles.

The mediaeval town grew up on the hill to the east of this around the Benedictine foundation of St Albans Abbey. This is the spot where tradition has it that St Alban, the first British Christian martyr, was beheaded sometime before AD 324. It was, at one time, the principal abbey in England and the first draft of Magna Carta was drawn up there, reflecting its political importance. The Abbey Church, now St Albans Cathedral (formally the Cathedral & Abbey Church of St Alban but still known locally as The Abbey) became the parish church when it was bought by the local people in 1553, soon after the priory was dissolved in 1539. It was made a cathedral in 1877 when the City Charter was granted. There is evidence that the original site was somewhat higher up the hill than the present building and there had certainly been successive abbeys before the current building was started in 1077.

St Albans School, a public school which occupies a site to the west of the Abbey and which includes the 14th century Abbey Gateway, was founded in AD 948 and is the only school in the English-speaking world to have educated a Pope (Adrian IV). It numbered amongst its buildings until comparatively recently a converted former hat factory, a link with the town's industrial past.

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