We assessed the prevalence of infection with Trypanosoma cruzi, parasite genotypes (discrete typing units, DTUs), and the host-feeding sources of domestic and peridomestic Triatoma infestans Klug and Triatoma eratyrusiformis Del Ponte in eight rural communities of the subandean Calchaqui valleys in northwestern Argentina. We sought to analyze their epidemiological role in the context of routine vector surveillance and control actions. Infection with T. cruzi was determined by optic microscopy or polymerase chain reaction (PCR) amplification of the hypervariable region of kinetoplast DNA minicircles. Parasite genotypes were identified through a multi PCR-based strategy. Bloodmeal contents were tested with a direct ELISA assay against nine antisera. Human sleeping quarters (domiciles) and peridomestic dry-shrub fences concentrated most of the T. infestans and T. eratyrusiformis infected with T. cruzi, respectively. The most frequent host-feeding sources of T. infestans were chickens (73.1%) in peridomiciles and humans (73.3%) in domiciles, whereas T. eratyrusiformis fed more often on cavid rodents (92.6%), which thrived in the dry-shrub fences. The main T. cruzi DTU identified in both vectors was T. cruzi I (TcI). Triatoma eratyrusiformis was implicated in the local circulation of TcI among cavies and perhaps mice, but infection with other typically domestic DTUs (TcVI and TcII/TcV/TcVI) indicated overlap between (peri)domestic transmission cycles in both vector species. Because dry-shrub fences were not targeted for routine insecticide spraying, they may act as sources of (peri)domestic reinfestation. Triatoma eratyrusiformis is an emergent secondary vector of T. cruzi and plays a significant role in the local transmission of T. cruzi.