The Kv3.3 potassium channel is expressed at high levels in the cerebellum and in auditory brainstem nuclei. Human mutations in Kv3.3 result in Spinocerebellar Ataxia 13 (SCA13), a condition associated with cerebellar atrophy and impaired auditory processing. The cytoplasmic C-terminus of Kv3.3 contains a proline-rich domain that is conserved in proteins that activate actin nucleation through the Arp2/3 complex. In addition to binding to the Arp2/3 complex, Kv3.3 channels interact directly with Hax-1, an apoptotic protein that regulates Arp2/3 actin nucleation. Wild-type Kv3.3 channels recruit Arp2/3 to the plasma membrane, resulting in the formation of a relatively stable cortical actin filament network. These Kv3.3-associated actin structures are required to prevent very rapid N-type channel inactivation during short depolarizations of the plasma membrane. In contrast, a human Kv3.3 SCA13 mutation within the proline-rich domain produce functional channels that fail to recruit Arp2/3 to the plasma membrane, resulting in growth cones with deficient actin veils in stem cell-derived neurons. In transfected cells, this mutation also results in abnormal trafficking of Hax-1 into multivesicular bodies and an increased rate of cell death. Our findings suggest that the Kv3.3 interaction with the Arp2/3 complex and Hax-1 generates stable actin structures that control ion channel inactivation gating and link the channel to signaling pathways that protect cerebellar neurons from apoptosis.