The actin-severing protein cofilin plays pivotal roles in actin cytoskeletal dynamics. Previously, our lab has shown that muscle-specific knockdown of Drosophila cofilin (DmCFL) leads to a progressive decline in larval muscle structure and function due to defective addition and maintenance of sarcomeres during growth. A similar deterioration is seen in the muscle disorder nemaline myopathy (NM) resulting from cofilin mutations. Given the importance of actin throughout the cell, I hypothesized that DmCFL knockdown would impact other aspects of muscle development. Consequently, I conducted an RNA sequencing analysis, which showed upregulation of genes associated with the neuromuscular junction (NMJ). The NMJ is the site of communication between the presynaptic motor neuron and postsynaptic muscle membrane. In this work, I found that DmCFL is enriched at the postsynaptic compartment, and its loss precipitates disorganization of F-actin prior to sarcomeric defects seen in the DmCFL KD model. Surprisingly, I did not observe significant changes in gross presynaptic Bruchpilot active zones or overall postsynaptic glutamate receptor levels. There is, however, a reduction and mislocalization of GluRIIA-containing glutamate receptors in DmCFL KD, resulting in a pronounced impairment in neurotransmission strength. These findings expand our understanding of cofilin’s roles in muscle to include NMJ structural development and suggest that NMJ defects may contribute to NM pathophysiology.