Non-ecological speciation is a common mode of speciation which occurs when allopatric lineages diverge in the absence of pronounced ecological differences. Yet, relative to other speciation mechanisms, non-ecological speciation remains understudied. Numerous damselfly clades are characterized as non-adaptive radiations (the result of several rounds of non-ecological speciation), but there are few damselfly lineages for which we have a detailed understanding of the spatiotemporal dynamics of divergence. Recent phylogeographic analyses demonstrate that American rubyspot damselflies (Hetaerina americanasensu lato) actually comprise at least two cryptic lineages that coexist sympatrically across most of Mexico. To broaden our understanding of the dynamics of diversification to other rubyspot lineages, we investigated the phylogeographic history of smoky rubyspot damselflies (Hetaerina titia) using genomic data collected across Central and North America. Unexpectedly, we found evidence of reproductive isolation between the highly genetically differentiated Pacific and Atlantic lineages ofH. titiain a narrow secondary contact zone on the Isthmus of Tehuantepec, Mexico. We then fit models of historical demography to bothH. americanasensu lato andH. titiato place these comparisons in a temporal context. Our findings indicate that Pacific and Atlantic lineages ofH. titiasplit more recently than the broadly sympatric lineages withinH. americanasensu lato, supporting key assumptions of the non-ecological speciation model and demonstrating that these two pairs of sister lineages are at different stages of the speciation cycle.