During development, synaptic exocytosis by cochlear hair cells is first initiated by patterned spontaneous Ca2+ spikes and, at the onset of hearing, by sound-driven graded depolarizing potentials. The molecular reorganization occurring in the hair cell synaptic machinery during this developmental transition still remains elusive. We characterized the changes in biophysical properties of voltage-gated Ca2+ currents and exocytosis in developing auditory hair cells of a precocial animal, the domestic chick. We found that immature chick hair cells (embryonic days 10–12) use two types of Ca2+ currents to control exocytosis: low-voltage-activating, rapidly inactivating (mibefradil sensitive) T-type Ca2+ currents and high-voltage-activating, noninactivating (nifedipine sensitive) L-type currents. Exocytosis evoked by T-type Ca2+ current displayed a fast release component (RRP) but lacked the slow sustained release component (SRP), suggesting an inefficient recruitment of distant synaptic vesicles by this transient Ca2+ current. With maturation, the participation of L-type Ca2+ currents to exocytosis largely increased, inducing a highly Ca2+ efficient recruitment of an RRP and an SRP component. Notably, L-type-driven exocytosis in immature hair cells displayed higher Ca2+ efficiency when triggered by prerecorded native action potentials than by voltage steps, whereas similar efficiency for both protocols was found in mature hair cells. This difference likely reflects a tighter coupling between release sites and Ca2+ channels in mature hair cells. Overall, our results suggest that the temporal characteristics of Ca2+ entry through T-type and L-type Ca2+ channels greatly influence synaptic release by hair cells during cochlear development.