Hypochilus is a relictual lineage of Nearctic spiders distributed disjunctly across the United States in three montane regions (California, southern Rocky Mountains, southern Appalachia). Phylogenetic resolution of species relationships in Hypochilus has been challenging, and conserved morphology coupled with extreme genetic divergence has led to uncertain species limits in some complexes. Here, Hypochilus interspecies relationships have been reconstructed and cryptic speciation more critically evaluated using a combination of ultraconserved elements, mitochondrial CO1 by-catch, and morphology. Phylogenomic data strongly support the monophyly of regional clades and support a ((California, Appalachia), southern Rocky Mountains) topology. In Appalachia, five species are resolved as four lineages (H. thorelli Marx, 1888 and H. coylei Platnick, 1987 are clearly sister taxa), but the interrelationships of these four lineages remain unresolved. The Appalachian species H. pococki Platnick, 1987 is recovered as monophyletic but is highly genetically structured at the nuclear level. While algorithmic analyses of nuclear data indicate many species (e.g., all H. pococki populations as species), male morphology instead reveals striking stasis. Within the California clade, nuclear and mitochondrial lineages of H. petrunkevitchi Gertsch, 1958 correspond directly to drainage basins of the southern Sierra Nevada, with H. bernardino Catley, 1994 nested within H. petrunkevitchi and sister to the southernmost basin populations. Combining nuclear, mitochondrial, geographical, and morphological evidence a new species from the Tule River and Cedar Creek drainages is described, Hypochilus xomotesp. nov. We also emphasize the conservation issues that face several microendemic, habitat-specialized species in this remarkable genus.