Triatominae are the largest radiation of haematophagous species within the true bugs (Hemiptera) and the sole vectors of Trypanosoma cruzi Chagas, the causative agent of Chagas disease, a neglected human disease that affects millions. We used a combined ultraconserved element (UCE) and ribosomal dataset from ethanol-preserved and pinned specimens in a museomics approach to elucidate the phylogenetic relationships among triatomines, including taxa of four of the five tribes with substantial representation of the Old World fauna. We conclude that: (i) Triatominae are monophyletic and Opisthacidius Berg is their predatory sister taxon; (ii) the three large genera (Rhodnius Stål, Triatoma Laporte and Panstrongylus Berg) are not monophyletic; (iii) Triatomini fall into nine well-supported clades, only two of which are identical in composition to previously recognized groups; and (iv) the Old World clade is deeply nested within Triatomini. Ancestral character state reconstructions of specific character traits provide insights into the evolutionary history of Triatominae.