Background: Triatoma dimidiata is a vector of the protozoan parasite Trypanosoma cruzi, the etiologic agent of Chagas disease. Phenotypic plasticity allows an organism to adjust its phenotype in response to stimuli or environmental conditions. Understanding the effect of T. cruzi on the phenotypic plasticity of its vectors, known as triatomines, has attracted great interest because of the implications of the parasite-triatomine interactions in the eco-epidemiology and transmission of the parasite. We investigated whether the infection of the vector with T. cruzi can change the antennal phenotype of sylvatic, domestic, and laboratory-reared populations of T. dimidiata. Methods: The abundance of each type of sensillum (bristles, basiconic, thick- and thin-walled trichoid) on the antennae of T. cruzi-infected and non-infected T. dimidiata reared in the laboratory or collected in sylvatic and domestic ecotopes were measured under light microscopy and compared using Kruskal–Wallis non-parametric tests and Permutational Multivariate Analysis of Variance. Results: We found significant differences between sensilla patterns of infected and non-infected insects within sylvatic and domestic populations. Conversely, we found no significant differences between sensilla patterns of infected and non-infected insects within the laboratory-reared population. Besides, our results show that the infection with T. cruzi affects the sexual dimorphism linked to antennal phenotype in sylvatic and domestic populations. Conclusion: These differences could be linked, for infected insects, to higher efficiency in the perception of odor molecules related to the search of distant mates and hosts and for flight dispersal in search of new habitats, and the possibility of a positive effect on population dynamics and on the vectorial transmission of T. cruzi.