In amniotes, head motions and tilt are detected by two types of vestibular hair cells (HCs) with strikingly different morphology and physiology. Mature type I HCs express a large and very unusual potassium conductance, g_K,L, which activates negative to resting potential, confers very negative resting potentials and low input resistances, and enhances an unusual non-quantal transmission from type I cells onto their calyceal afferent terminals. Following clues pointing to K_V1.8 (Kcna10) in the Shaker K channel family as a candidate gK,L subunit, we compared whole-cell voltage-dependent currents from utricular HCs of K_V1.8-null mice and littermate controls. We found that K_V1.8 is necessary not just for g_K,L but also for fast-inactivating and delayed rectifier currents in type II HCs, which activate positive to resting potential. The distinct properties of the three K_V1.8-dependent conductances may reflect different mixing with other K_V subunits that are reported to be differentially expressed in type I and II HCs. In K_V1.8-null HCs of both types, residual outwardly rectifying conductances include K_V7 (Knq) channels. Current clamp records show that in both HC types, K_V1.8-dependent conductances increase the speed and damping of voltage responses. Features that speed up vestibular receptor potentials and non-quantal afferent transmission may have helped stabilize locomotion as tetrapods moved from water to land.