Anopheles arabiensis is a highly adaptable member of the An. gambiae complex. Its flexible resting behaviour and diverse feeding habits make conventional vector control methods less effective in controlling this species. Another emerging challenge is its adaptation to breeding in polluted water, which impacts various life history traits relevant to epidemiology. The gut microbiota of mosquitoes play a crucial role in their life history, and the larval environment significantly influences the composition of this bacterial community. Consequently, adaptation to polluted breeding sites may alter the gut microbiota of adult mosquitoes. This study aimed to examine how larval exposure to metal pollution affects the gut microbial dynamics of An. arabiensis adults. Larvae of An. arabiensis were exposed to either cadmium chloride or copper nitrate, with larvae reared in untreated water serving as a control. Two laboratory strains (SENN: insecticide unselected, SENN-DDT: insecticide selected) and F1 larvae sourced from KwaZulu-Natal, South Africa, were exposed. The gut microbiota of the adults were sequenced using the Illumina Next Generation Sequencing platform and compared. Larval metal exposure affected alpha diversity, with a more marked difference in beta diversity. There was evidence of core microbiota shared between the untreated and metal-treated groups. Bacterial genera associated with metal tolerance were more prevalent in the metal-treated groups. Although larval metal exposure led to an increase in pesticide-degrading bacterial genera in the laboratory strains, this effect was not observed in the F1 population. In the F1 population, Plasmodium-protective bacterial genera were more abundant in the untreated group compared to the metal-treated group. This study therefore highlights the importance of considering the larval environment when searching for local bacterial symbionts for paratransgenesis interventions.