The site of Whitchurch was first occupied by a Roman fort of the late second century, around which settlement developed; known as Mediolanum, it was situated on that part of Watling Street connecting Chester and Wroxeter. Though the Roman settlement was probably abandoned, Watling Street continued in use into the Middle Ages and settlement at the site of Whitchurch – higher ground between two small valleys – may have resumed before the Conquest. Whitchurch is not mentioned in Domesday Book, but it is thought to have been within the manor of Weston, where 23 villagers are mentioned in 1086 and a church was founded a little later, from which the Latin name of Blancmuster was given to the settlement, as at Oswestry; although the church is dedicated to an Anglo-Saxon saint, there is not yet any evidence a pre-Conquest church stood on the site. In 1086 the manor was held of Earl Roger by William de Warenne, his only Shopshire property, although he held manors directly of the king in a number of other counties. His family was connected to those of the earls of both Shrewsbury and Hereford, as well as to the Conqueror and to the Mortimers; he was made Earl of Surrey only months before his death in 1088. The successors to the earldom were more focused on their estates elsewhere in England, and Whitchurch did not follow the main line of descent; it came into the hands of William Fitz-Ranulf, who may perhaps have been of a cadet branch of the house of Warenne.

A castle is heard of at Whitchurch in 1199, when under repair byWilliam Fitz-Ranulf with royal funding; but, like the nearby church (on the other side of Watling Street), the castle may have existed for over a century – likely put up by William de Warenne when he was called upon to share in the defence of the Welsh frontier. If the earliest castle was of wood, it had certainly been rebuilt in stone by the fourteenth century, and was still being kept in repair in 1384, though perhaps not in the fifteenth century, with Wales pacified. Archaeology has evidenced twelfth century settlement near castle and church. Eyton argued that Fitz-Ranulf also had property in East Anglia and Middlesex, although there were several persons of this name living around the same period. Around 1260 the male line of the family was extinguished, leaving three daughters as co-heirs, one of whom was married to Robert le Strange (of the family associated with Knockin, Ellesmere, and Ruyton); his son Fulk inherited one of the three shares of Whitchurch, and subsequently acquired the other two shares, thus becoming sole lord, as sub-tenant of Earl Warenne.

Though there is no surviving record of a market licence, court documents of the late thirteenth century describe Whitchurch as possessing market and fair; in one case (1284/85) appellants declared they knew not by what right, but in another a royal charter of Richard I to William Fitz-Ranulf was presented in evidence of a market grant. When first evidenced, the market was held on a Wednesday, but by the late fourteenth century there were Monday and Friday markets. In 1362 John le Strange, grand-son of Fulk, received grant of an October fair at Whitchurch. In 1377 the town came into the hands of the Talbot family, destined for the earldom of Shrewsbury within a generation.

The castle was on the west side of the site and the church just north-east of it, the west side of the churchyard fronted the High Street. The suspicion is that, around 1190, a planned town was laid out on either side of that street (part of Watling Street, which headed south-eastwards past castle and church) and was protected with roughly U-shaped ditch and rampart defences, running on about the same line as those of the Roman fort, but now linked to the castle bailey; pottery within the ditch dated to the twelfth century. The ditch was backfilled with clay – perhaps partly by levelling the rampart, but mainly material that may have come from a site commemorated by the name Claypit Street – in the fourteenth century. The shape of these medieval defences became crystallized in the street pattern. The street just within their west side was known as Newtown, referring to an expansion of the town in the fourteenth century. The High Street ran roughly through the centre of this defended area; where it exited that area, at the north end, the name changed to Bargates, suggesting a fortified entrance, while just beyond the southern end of the enclosure, presumably where another gateway was in place, it terminated at a junction with a looping road. Running between the High Street and Newtown was a narrow lane whose name of Pepper Street was documented towards the close of the Middle Ages, and where a pebbled medieval surface was found; it may have been created when the planned expansion of Newtown was created. The High Street was similarly paved with sand-embedded pebbles placed end-downwards. Bargates and Claypit Street were also areas of late medieval expansion, probably unplanned, while other streets heading away from the defensive enclosure may have seen some expansion too; expansion continued into the post-medieval period.

The medieval market was probably held along the High Street. By the Late Middle Ages, as the town expanded beyond its defences, a funnel-shaped area at the junction at the south end of the High Street, known as the Bull Ring – a name associated with marketplaces in a number of towns – was included within the market area.

Whitchurch was close enough to salt-producing centres that it could have augmented commerce in agricultural produce from the vicinity with a role in distribution of salt – a role documented in the thirteenth century. Its tax assessment in 1334 shows Whitchurch prospering, and expansion during that century is testimony to the same. This growth may help explain the fair licence of 1362 and the increase from one to two weekly market days, although the licence might just have formalized an unlicensed fair already in existence. Whitchurch continued to thrive in the post-medieval period as a medium-sized market town.