[4] The suburbs include the former parish of Prendergast,[5] Albert Town and the residential and industrial areas of Withybush (housing, retail parks, hospital, airport and showground).

The majority of the town, comprising the old parishes of St. Mary, St. Martin and St. Thomas, lies on the right (west) bank of the river.

At this point, a pair of sandstone ridges extending from east to west and separated by a deep, narrow valley, are cut through by the Western Cleddau.

On the southern spur, the High Street ascends steeply from the river and forms the core of St Mary's parish.

In addition to the four ancient parish churches, the remains of an Augustinian priory are visible at the southern edge of the town.

South Pembrokeshire is known as 'Little England Beyond Wales', but because the markets traded with Welsh farmers in the north and east, there has always been a significant Welsh-speaking influence.

The suburb of Prendergast seems to have originated as an extramural Welsh dormitory, dating from the times when all agricultural trade had to pass through the borough, and the fearful Normans before the destruction of Anglo-Norman power in 1136 tried to prevent Welshmen bearing arms from entering within the castle walls after nightfall.

The strategic position of Haverfordwest with its defensive bluff overlooking the lowest fordable point on the western Cleddau and accessible to sea traffic would have required a Roman presence, probably modest in scale, from the 1st century AD to protect supplies to and from the coast, e.g. the Roman legionary headquarters at Caerleon were roofed with slates from the lower slopes of the Preseli Hills.

In the 1920s Sir Mortimer Wheeler partially excavated a Roman dwelling or villa at Wolfscastle; work was restarted in 2002 by Professor Merroney.

The Flemish presence, reputed to result from floods in the Low Countries, was more likely to have consisted initially of Flemish mercenaries originally in the invading army of William the Conqueror, who in reward for their part in William's victory were granted lands in parts of Northern Britain, and in Wales in the Gower, and Geraldus Cambrensis recorded their presence in the Hundred of Roose in Pembrokeshire.

The precarious position of Normans and Flemings was demonstrated in 1136 when the Normans, having already lost 500 men in battle at Loughor, re-recruited from Lordships from all over South Wales and led by Robert fitz Martin at Crug Mawr near Cardigan attacked Owain Gwynedd and his army.

Ranulf Higden, in his Polychronicus, records the Flemings as extinct in Pembrokeshire by 1327 but Flemish mercenaries reappear in 1400 when at the behest of Henry IV they joined an army of 1,500 English settlers who marched north from Pembrokeshire to attack the army of Owain Glyndŵr at Mynydd Hyddgen.

The attack was repulsed with heavy casualties and legend has it that English prisoners were spared but surviving Flemish mercenaries were massacred or sold into slavery.

Haverfordwest rapidly grew, initially around the castle and St Martin's Church (the settlement being called Castletown), then spreading into the High Street area.

It immediately became the capital of the hundred of Roose (part of Little England beyond Wales), and because of its pivotal position, the commercial centre of western Dyfed, which it has remained to this day.

It received its first marcher charter from William Marshall, 1st Earl of Pembroke sometime between 1213 and 1219, and obtained the lucrative trading privileges of an English borough.

In 1545, the town was designated a county corporate by Henry VIII, with the aim of supporting a campaign against piracy in local waters.

[14] In common with other large towns in Europe, Haverfordwest was hit hard by the Black Death in 1348, suffering both depopulation (perhaps by more than 50%) and diminution of trade.

[18] Haverfordwest today has the air of a typical small country market town, but the centre still conveys the feel of the important mediaeval borough.

In October 2022, the remains of 307 people, including children, were unearthed by archaeologists working on the remnants of a medieval priory found beneath the old Ocky White building, a former department store which closed in 2013.

[21] For local government purposes the community of Haverfordwest comprises five wards: Castle, Prendergast, Portfield, Priory and Garth.

[27] In the UK Parliament, Haverfordwest is part of the Mid and South Pembrokeshire constituency, currently represented by Henry Tufnell of Welsh Labour.

[41] Haverfordwest had a medieval guildhall which stood at the top (west end) of High Street in front of St Mary's Church.

In 1871 the borough acquired newly built premises at 1 St Mary's Lane to serve as the council's offices and meeting place.

[3] In accordance with its status as a sub-regional hub-town, Haverfordwest continues to serve as Pembrokeshire's principal commercial and retail centre.

[56] The development of the riverside shopping centre in Withybush on the outskirts of the town includes Marks & Spencer in 2010[57] and Debenhams in 2013.

Concerns about the relative decline of the historic town centre compared to the growth of the retail centre at Withybush led to Welsh historian John Davies expressing his concern that Haverfordwest is becoming "a medieval town surrounded by tin sheds".

[citation needed] Schools and colleges in Haverfordwest: Haverfordwest County play association football in the Cymru Premier (the top tier of Welsh football) at Bridge Meadow Stadium, while Merlins Bridge play in the local Pembrokeshire League.