No medieval walls predate the late sixteenth century here; in 1584 the town was formally described as 'lying open to all attempts', and its provost and gaol constable were granted two annual fairs specifically so that the tolls could be channelled into enclosing and fortifying the settlement. What actually went up is still unclear: some references point to stone walls, others to earthen ramparts, and the 1641 survey of the town mentions both a 'rampier', meaning an earthen embankment, on the north side and a town wall on the south, suggesting that the defences may have been a hybrid of earth and stone depending on where you stood.

The paper trail for these defences is fragmentary but revealing. As early as 1583 Queen Elizabeth directed that fair revenues be put into a treasury and applied 'about the enclosing and fortifying of the town'. By 1609 an inquisition into the estate of Thomas Hopp, Constable of Mullingar, noted the existence of a west gate, giving the structure at least one named entrance. The 1641 survey of the town places individual properties in relation to 'the walls of the said town' on both the north and south, and refers to a 'Motegate' or Motte Gate near the town's Anglo-Norman motte, a large earthen mound on which a stone castle had been built. Whether this gate pierced the town defences proper or simply opened into the castle's courtyard is uncertain. The 1656 Down Survey map shows the town as a compact oval on the banks of the River Brosna, with what appears to be a crenellated wall along the north side, which would imply battlemented stonework at least in that section. Six openings in the defences seem to correspond with the roads radiating out of town, though whether each had a formal gatehouse is unknown. A generation later, during the Williamite Wars of 1690 to 1691, a second outer ring of earthwork fortifications was thrown up around the existing circuit; a map drawn by Richards in 1691 shows a double concentric line of defences with four forts projecting from the inner ring, and what may have been a star-shaped fort enclosing All Saints' parish church. The inner circuit enclosed roughly 15 hectares, the outer ring between 20 and 25 hectares.

The defences themselves are long gone, but their outline can still be read in the modern town. Bishop's Gate Street and Church Street, shown on the 1838 Ordnance Survey map as 'Back of the Town', almost certainly follow the northern line of the old enclosure. The River Brosna, which curves around the eastern side, served as a natural boundary and may have doubled as a defensive feature on the south as well. The western limit of the historic town corresponds roughly with the old Linen Street, now Dominick Street. Walking these edges today, you are tracing a boundary first drawn when Elizabethan administrators decided that a town placed on the main road from Dublin to Connacht could no longer afford to remain undefended.