Medekšiai has been known since the 15th century. King Jogaila presented the village to a certain Proszczy whose nickname was Medekša. Pranciškus Medekša, a judge of Kovensky Uyezd, had been native of this family. In the end of the 19th century Medekšiai was a property of the Geištarai. Činkiai village and Slabadėlė folwark belonged to the Medekšiai Manor.
During the Soviet era, Medekšiai was a subsidiary settlement of the "Spike" kolkhoz.