Synapse formation is tightly associated with neuronal excitability. We found striking synaptic overgrowth caused byDrosophilaK+-channel mutations of theseizureandslowpokegenes, encoding Erg and Ca2+-activated large-conductance (BK) channels, respectively. These mutants display two distinct patterns of “satellite” budding from larval motor terminus synaptic boutons. Double-mutant analysis indicates that BK and Erg K+channels interact with separate sets of synaptic proteins to affect distinct growth steps. Post-synaptic L-type Ca2+channels, Dmca1D, and PSD-95-like scaffold protein, Discs large, are required for satellite budding induced byslowpokeandseizuremutations. Pre-synapticcacophonyCa2+channels and the NCAM-like adhesion molecule, Fasciclin II, take part in a maturation step that is partially arrested byseizuremutations. Importantly,slowpokeandseizuresatellites were both suppressed byrutabagamutations that disrupt Ca2+/CaM-dependent adenylyl cyclase, demonstrating a convergence of K+channels of different functional categories in regulation of excitability-dependent Ca2+influx for triggering cAMP-mediated growth plasticity.