The C. elegans AWC olfactory neuron pair communicates to specify asymmetric subtypes, AWCOFF and AWCON across the left-right axis. Intercellular communication between AWC and other neurons in a transient NSY-5 gap junction network antagonizes voltage-activated Ca2+ channels, UNC-2 (CaV2) and EGL-19 (CaV1), in the AWCON cell, but how Ca2+ signaling is downregulated by NSY-5 is only partly understood. We show that voltage- and Ca2+ -activated SLO BK potassium channels mediate gap junction signaling to inhibit Ca2+ pathways for asymmetric AWC differentiation. Activation of vertebrate SLO-1 channels causes transient membrane hyperpolarization, making it an important negative feedback system for Ca2+ entry through voltage-activated Ca2+ channels. Consistent with the physiological roles of SLO-1, our genetic results suggest that slo-1 acts downstream of nsy-5 to inhibit Ca2+ channel-mediated signaling to specify AWCON. We also show for the first time that SLO-2 BK channels are important for AWC asymmetry and act redundantly with SLO-1 to inhibit Ca2+ signaling. nsy-5-dependent asymmetric expression of slo-1 and slo-2 in the AWCON neuron is necessary and sufficient for AWC asymmetry. SLO-1 and SLO-2 localize close to UNC-2 and EGL-19 in AWC, consistent with functional coupling between these channels in AWC asymmetry. Furthermore, slo-1 and slo-2 regulate the localization of synaptic markers in AWC neurons to control AWC asymmetry. We also identify the requirement of bkip-1, which encodes a previously identified auxiliary subunit of SLO-1, for slo-1 and slo-2 function in AWC asymmetry. Together, these results provide an unprecedented molecular link between gap junctions and Ca2+ pathways for terminal differentiation of olfactory neurons. To identify the genes required for slo-1 function in inhibiting Ca2+ signaling for promoting AWCON, we performed a non-biased forward genetic screen to isolate mok (modifier of K+ channel) mutants that suppress the slo-1(gf) 2AWCON phenotype. From about 6000 genomes screened, we identified 16 new mok mutants that define genes required for slo-1 function in promoting AWCON. We have identified the mutations responsible for these mok phenotypes using whole genome sequencing (kindly performed by Oliver Hobert’s group). Molecular characterization of these mok genes will provide insight into how K+ channels and Ca2+ channels may interact to coordinate stochastic AWC asymmetry.