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Abstract The recognition and delineation of cryptic species remains a perplexing problem in systematics, evolution, and species delimitation. Once recognized as such, cryptic species complexes provide fertile ground for studying genetic divergence within the context of phenotypic and ecological divergence (or lack thereof). Herein we document the discovery of a new cryptic species of trapdoor spider,Promyrmekiaphila korematsuisp. nov. Using subgenomic data obtained via target enrichment, we document the phylogeography of the California endemic genusPromyrmekiaphilaand its constituent species, which also includesP. clathrataandP. winnemem. Based on these data we show a pattern of strong geographic structuring among populations but cannot entirely discount recent gene flow among populations that are parapatric, particularly for deeply diverged lineages withinP. clathrata. The genetic data, in addition to revealing a new undescribed species, also allude to a pattern of potential phenotypic differentiation where species likely come into close contact. Alternatively, phenotypic cohesion among genetically divergentP. clathratalineages suggests that some level of gene flow is ongoing or occurred in the recent past. Despite considerable field collection efforts over many years, additional sampling in potential zones of contact for both species and lineages is needed to completely resolve the dynamics of divergence inPromyrmekiaphilaat the population–species interface.