Genetic and morphological structure of vector populations are useful to identify panmictic groups, reinfestation sources and minimal units for control interventions. Currently, no studies have integrated genetic and morphometric data in Triatoma infestans (Hemiptera: Reduviidae), one of the main vectors of Trypanosoma cruzi. We characterized the genetic and phenotypic structure of T. infestans at a small spatial scale (2–8 km), identified potential migrants and compared flight-related traits among genetic groups and between migrant and non-migrant insects in a well-defined area without insecticide spraying in the previous 12 years. We obtained microsatellite genotypes (N = 303), wing shape and size (N = 164) and body weight-to-length ratios (N = 188) in T. infestans from 11 houses in Pampa del Indio, Argentine Chaco. The uppermost level of genetic structuring partially agreed with the morphological groups, showing high degrees of substructuring. The genetic structure showed a clear spatial pattern around Route 3 and one genetic group overlapped with an area of persistent infestation and insecticide resistance. Females harboured more microsatellite alleles than males, which showed signs of isolation-by-distance. Wing shape discriminant analyses of genetic groups revealed low reclassification scores whereas wing size differed among genetic groups for both sexes. Potential migrants (8%) did not differ from non-migrants in sex, ecotope, wing shape and size. However, male migrants had lower W/L than non-migrants suggesting poorer nutritional state. Our findings may contribute to the understanding of population characteristics, dispersal dynamics and ongoing elimination efforts of T. infestans.