How and when sensory hair cells acquire the remarkable ability to detect and transmit mechanical information carried by sound and head movements has not been illuminated. Previously, we defined the onset of mechanotransduction in embryonic hair cells of mouse vestibular organs to be at approximately embryonic day 16 (E16). Here we examine the functional maturation of hair cells in intact sensory epithelia excised from the inner ears of embryonic mice. Hair cells were studied at stages between E14 and postnatal day 2 using the whole-cell, tight-seal recording technique. We tracked the developmental acquisition of four voltage-dependent conductances. We found a delayed rectifier potassium conductance that appeared as early as E14 and grew in amplitude over the subsequent prenatal week. Interestingly, we also found a low-voltage-activated potassium conductance present at E18, approximately 1 week earlier than reported previously. An inward rectifier conductance appeared at approximately E15 and doubled in size over the next few days. We also noted transient expression of a voltage-gated sodium conductance that peaked between E16 and E18 and then declined to near zero at birth. We propose that hair cells undergo a stereotyped developmental pattern of ion channel acquisition and that the precise pattern may underlie other developmental processes such as synaptogenesis and functional differentiation into type I and type II hair cells. In addition, we find that the developmental acquisition of basolateral conductances shapes the hair cell receptor potential and therefore comprises an important step in the signal cascade from mechanotransduction to neurotransmission.