Glial cells are emerging as important regulators of synapse formation, maturation, and plasticity through the release of secreted signaling molecules. Here we use chromatin immunoprecipitation along withDrosophilagenomic tiling arrays to define potential targets of the glial transcription factorReversed polarity(Repo). Unexpectedly, we identifiedwingless(wg), a secreted morphogen that regulates synaptic growth at theDrosophilalarval neuromuscular junction (NMJ), as a potential Repo target gene. We demonstrate that Repo regulateswgexpressionin vivoand that local glial cells secrete Wg at the NMJ to regulate glutamate receptor clustering and synaptic function. This work identifies Wg as a novelin vivoglial-secreted factor that specifically modulates assembly of the postsynaptic signaling machinery at theDrosophilaNMJ.