Sensory hair cells convert mechanical motion into chemical signals. Otoferlin, a six-C2 domain transmembrane protein linked to deafness in humans, is hypothesized to play a role in synaptic vesicle exocytosis at hair cell ribbon synapses. To date however, otoferlin has been studied almost exclusively in mouse models which are technically challenging due to the inaccessibility of their hair cells and reluctance to genetic manipulation, and no rescue experiments have been reported. To overcome these challenges, we have developed zebrafish as a model for studying otoferlin function, and report the first otoferlin rescue experiments. We found that larval zebrafish have two otoferlin genes, otoferlin a and otoferlin b that are expressed early in development and are restricted to sensory hair cells and the midbrain. Knockdown of the otoferlin genes resulted in hearing and balance defects, and a phenotype associated with a looping and circular swimming pattern. Otoferlin morphants also had uninflated swim bladders. Microscopy revealed that otoferlin localized to both the apical and synaptic basolateral side of the cell and that knockdown resulted in abnormal presynaptic structures; namely changes in synaptic ribbon distribution and synaptic vesicle VGlut3 localization. Fluorescent mCLING dye loading experiments suggest that the loss of otoferlin also results in defective synaptic vesicle exocytosis and recycling. RNA-seq studies we have conducted provide a “big picture” view of otoferlin’s impact on zebrafish, and implicate otoferlin-related signaling in a variety of physiological processes extending beyond hearing. Rescue experiments conducted with mouse otoferlin completely restored hearing, balance, and inflation of the swim bladder. Remarkably, truncated forms of otoferlin retaining the C-terminal C2F domain also rescued the otoferlin knockdown phenotype, while the individual N-terminal C2A domain did not. We conclude that otoferlin plays an evolutionarily conserved role in vertebrate hearing and that truncated forms of mouse otoferlin can rescue hearing and balance.