Voltage-gated sodium channels (Na V s) are central elements of cellular excitation. Notwithstanding advances from recent bacterial Na V (BacNa V ) structures, key questions about gating and ion selectivity remain. Here, we present a closed conformation of Na V Ae1p, a pore-only BacNa V derived from Na V Ae1, a BacNa V from the arsenite oxidizer Alkalilimnicola ehrlichei found in Mono Lake, California, that provides insight into both fundamental properties. The structure reveals a pore domain in which the pore-lining S6 helix connects to a helical cytoplasmic tail. Electrophysiological studies of full-length BacNa V s show that two elements defined by the Na V Ae1p structure, an S6 activation gate position and the cytoplasmic tail "neck", are central to BacNa V gating. The structure also reveals the selectivity filter ion entry site, termed the "outer ion" site. Comparison with mammalian voltage-gated calcium channel (Ca V ) selectivity filters, together with functional studies, shows that this site forms a previously unknown determinant of Ca V high-affinity calcium binding. Our findings underscore commonalities between BacNa V s and eukaryotic voltage-gated channels and provide a framework for understanding gating and ion permeation in this superfamily.