Conditions experienced during larval development of holometabolous insects can affect adult traits, but whether differences in the bacterial communities of larval development sites contribute to variation in the ability of insect vectors to transmit human pathogens is unknown. We addressed this question in the mosquito Aedes aegypti, a major arbovirus vector breeding in both sylvatic and domestic habitats in Sub-Saharan Africa. Targeted metagenomics revealed differing bacterial communities in the water of natural breeding sites in Gabon. Experimental exposure to different native bacterial isolates during larval development resulted in significant differences in pupation rate and adult body size but not life span. Larval exposure to an Enterobacteriaceae isolate resulted in decreased antibacterial activity in adult hemolymph and reduced dengue virus dissemination titer. Together, these data provide the proof of concept that larval exposure to different bacteria can drive variation in adult traits underlying vectorial capacity. Our study establishes a functional link between larval ecology, environmental microbes, and adult phenotypic variation in a holometabolous insect vector.