Voltage-gated Na⁺ channel (VGSC) β1 subunits regulate cell–cell adhesion and channel activity in vitro. We previously showed that β1 promotes neurite outgrowth in cerebellar granule neurons (CGNs) via homophilic cell adhesion, fyn kinase, and contactin. Here we demonstrate that β1-mediated neurite outgrowth requires Na⁺ current (I_Na) mediated by Na_v1.6. In addition, β1 is required for high-frequency action potential firing. Transient I_Na is unchanged in Scn1b (β1) null CGNs; however, the resurgent I_Na, thought to underlie high-frequency firing in Na_v1.6-expressing cerebellar neurons, is reduced. The proportion of axon initial segments (AIS) expressing Na_v1.6 is reduced in Scn1b null cerebellar neurons. In place of Na_v1.6 at the AIS, we observed an increase in Na_v1.1, whereas Na_v1.2 was unchanged. This indicates that β1 is required for normal localization of Na_v1.6 at the AIS during the postnatal developmental switch to Na_v1.6-mediated high-frequency firing. In agreement with this, β1 is normally expressed with α subunits at the AIS of P14 CGNs. We propose reciprocity of function between β1 and Na_v1.6 such that β1-mediated neurite outgrowth requires Na_v1.6-mediated I_Na, and Na_v1.6 localization and consequent high-frequency firing require β1. We conclude that VGSC subunits function in macromolecular signaling complexes regulating both neuronal excitability and migration during cerebellar development.