The corsair bugs (Reduviidae: Peiratinae) are a medium-sized subfamily of assassin bugs with over 340 species described worldwide. Individuals in the subfamily exhibit putative aposematic color patterns, several of which occur in different genera suggesting a complex evolutionary history of color patterns in the group. Along with their striking appearance, their mating behaviors are unique, being one of the only reduviids with asymmetric male genitalia and accordingly modified mating position. Here, we infer the first robust phylogenetic hypothesis across Peiratinae using nuclear, mitochondrial, and anchored hybrid enrichment loci (~178 kbp). Based on this analysis we recover a well-supported phylogeny that infers a paraphyletic Sirthenea and Rasahus, and polyphyletic Ectomocoris, thus highlighting that the speciose genera of Peiratinae need taxonomic revision. We used this phylogenetic hypothesis to reconstruct the ancestral character state of color patterns and male and female genitalic characters and observe multiple gains and losses of 1) putative aposematic color patterns, 2) male extragenital processes, 3) male asymmetric median abdominal carina, and 4) putative interlocking structures on the first valvulae. These results provide a comparative framework for further behavioral and functional exploration of these traits to better understand their evolutionary roles.