Archaeological finds in the area date local habitation back to Neolithic times. Under the Romans a link was made to it from the road between Cassel and Aardenburg. In the time of the Franks it appeared under the name Pupurningahem and was made subject to the ecclesiastical benefice of Saint Omer in the mid-7th century. The Count of Flanders, Dietrich of Alsace, granted the town a charter in 1147 at the request of the abbot. From this time it began to thrive as a cloth-making centre and, in order to accommodate the growing population, the churches of Saint John and of Our Lady were added in 1290 to the already existing Sint-Bertinuskerk.
In 1322 Louis de Nevers forbade cloth-making outside Ieper, which inclined the citizens to join the revolt against him the following year. Nor did they ever submit to this restraint on their prosperity and were forever finding new ways to evade the restriction. Their resistance during this period gained them the nickname of keikoppen (cobble-heads), a term first recorded in 1341, when the Ieper militia took revenge on the town.
During the disturbances associated with the Hundred Years War, Poperinge suffered from the shifting allegiances of the Counts of Flanders and their commercial consequences. When they supported the French, the wool trade with England was interrupted. In the course of the consequent revolt, the town was sacked and burned by French troops in 1382. Then in 1436 it suffered the same fate from an English army. In 1513, at a time of declining prosperity, much of the town was again destroyed by fire and once more in 1563. During this period Poperinge was stirred up to support the Protestant cause and took part in the iconoclastic fury of 1566. It was in the consequent fighting and persecution that the town and its trade were finally ruined.
Matters were made worse by the wars between the French and the Dutch for control of the region. By the treaty of Nijmegen in 1678 the town passed into French