Key points Sound and balance information is detected and processed by sensory hair cells in the auditory and vestibular organs, respectively. The zebrafish represents a potentially powerful model organism in which to investigate sensory encoding by hair cells because of its accessibility for in vivo studies and its pliable genetics. Our current understanding of hair cell biophysics in the developing zebrafish is very limited. In this study, we used in vivo and near‐physiological in vitro recordings to measure basolateral membrane currents, voltage changes and synaptic activity in hair cells in the developing and mature zebrafish. We found that the biophysical profile of lateral line hair cells in the zebrafish changes from the larval to the juvenile stage, and that juvenile neuromasts contain a much higher proportion of mature cells. These results demonstrate the potential of the zebrafish for investigating the mechanisms of signal encoding and transmission by hair cells. Abstract Hair cells detect and process sound and movement information, and transmit this with remarkable precision and efficiency to afferent neurons via specialized ribbon synapses. The zebrafish is emerging as a powerful model for genetic analysis of hair cell development and function both in vitro and in vivo. However, the full exploitation of the zebrafish is currently limited by the difficulty in obtaining systematic electrophysiological recordings from hair cells under physiological recording conditions. Thus, the biophysical properties of developing and adult zebrafish hair cells are largely unknown. We investigated potassium and calcium currents, voltage responses and synaptic activity in hair cells from the lateral line and inner ear in vivo and using near‐physiological in vitro recordings. We found that the basolateral current profile of hair cells from the lateral line becomes more segregated with age, and that cells positioned in the centre of the neuromast show more mature characteristics and those towards the edge retain a more immature phenotype. The proportion of mature‐like hair cells within a given neuromast increased with zebrafish development. Hair cells from the inner ear showed a developmental change in current profile between the juvenile and adult stages. In lateral line hair cells from juvenile zebrafish, exocytosis also became more efficient and required less calcium for vesicle fusion. In hair cells from mature zebrafish, the biophysical characteristics of ion channels and exocytosis resembled those of hair cells from other lower vertebrates and, to some extent, those in the immature mammalian vestibular and auditory systems. We show that although the zebrafish provides a suitable animal model for studies on hair cell physiology, it is advisable to consider that the age at which the majority of hair cells acquire a mature‐type configuration is reached only in the juvenile lateral line and in the inner ear from >2 months after hatching.