Sound encoding is mediated by Ca²⁺influx-evoked release of glutamate at the ribbon synapse of inner hair cells. Here we studied the role of ATP in this process focusing on Ca²⁺current through Ca_V1.3 channels and Ca²⁺homeostasis in mouse inner hair cells. Patch-clamp recordings and Ca²⁺imaging demonstrate that hydrolyzable ATP is essential to maintain synaptic Ca²⁺influx in inner hair cells via fueling Ca²⁺-ATPases to avoid an increase in cytosolic [Ca²⁺] and subsequent Ca²⁺/calmodulin-dependent inactivation of Ca_V1.3 channels.