Degenerin/Epithelial Sodium Channels (DEG/ENaCs) represent a diverse family of animal-specific ion channels that play an important role in regulating ionic gradients across epithelial barriers. Members of the family are also enriched in neural tissues. However, in contrast to epithelial tissues, their neurophysiological functions are still mostly unknown. The Drosophila genome encodes an exceptionally large number of DEG/ENaC subunits termed pickpocket 1-31 (ppk) family. By using genetic, neurophysiological, and behavioral approaches, we demonstrate that the DEG/ENaC channel subunit PPK29 contributes specifically to postsynaptic modulation of excitatory synaptic transmission at the larval neuromuscular junction (NMJ). We show that ppk29 is necessary in the muscle for normal response to spontaneous, but not stimulus-evoked, neurotransmitter release, without an apparent impact on gross synaptic development or morphology. In addition, mutations in ppk29 lead to impaired coordinated movement required for stereotypic larval rolling behavior. Together, our data indicate a novel postsynaptic function for members of the DEG/ENaC family of ion channels.