The nervous system is a complex network of cells whose interactions provide circuitry that enables an organism to perceive and move through its environment. Both neuron-neuron and neuron-non-neuronal cell communications are essential for proper nervous system function. Considerable research has focused on communication between motor neurons and muscles, albeit the molecular basis of glial cell-neuron communication is still not well understood and its elucidation will advance our understanding of complex neural responses and abnormalities of the nervous system that arise when such communication fails. In Drosophilamelanogaster, retrograde BMP signaling, activated by muscle-expressed Gbb (BMP5/6/7), has been shown to influence synaptic growth, function and plasticity. Here, we report Gbb also acts from glial cells to initiate signaling in motor neurons, an additional source of BMP ligand required for synaptic growth at the neuromuscular junction (NMJ). Furthermore, we find Dpp (BMP2/4), expressed in a subset of motor neurons (RP2 and aCC), facilitates NMJ growth through autocrine neuronal signaling and its expression in RP2 versus aCC motor neurons appears tightly controlled via an autoregulatory loop. Dpp also initiates neuron to glial cell signaling, but not neuron-neuron signaling to neighboring motor neurons. Together, our findings demonstrate that bi-directional communication between glia and neurons requires two different BMP ligands. Gbb, broadly expressed in glia, as well as muscles, and Dpp, from a discrete set of neurons, activate Smad-dependent BMP signaling in motor neurons to control synapse size.