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Abstract Metazoans rely on interactions with microorganisms through multiple life stages. For example, developmental trajectories of mosquitoes can vary depending on the microorganisms available during their aquatic larval phase. However, the role that the local environment plays in shaping such host-microbe dynamics and the consequences for the host organism remain inadequately understood. Here, we examine the influence of abiotic factors, locally available bacteria, and their interactions on the development and associated microbiota of the mosquito Aedes albopictus. Our findings reveal that leaf detritus infused into the larval habitat water, sourced from native Hawaiian tree ‘ōhi‘a lehua Metrosideros polymorpha, invasive strawberry guava Psidium cattleianum, or a pure water control, displayed a more substantial influence than either temperature variations or simulated microbial dispersal regimes on bacterial community composition in adult mosquitoes. However, specific bacteria exhibited divergent patterns within mosquitoes across detrital infusions that did not align with their abundance in the larval habitat. Specifically, we observed a higher relative abundance of a Chryseobacterium sp. strain in mosquitoes from the strawberry guava infusion than the pure water control, whereas the opposite trend was observed for a Pseudomonas sp. strain. In a follow-up experiment, we manipulated the presence of these two bacterial strains and found larval developmental success was enhanced by including the Chryseobacterium sp. strain in the strawberry guava infusion and the Pseudomonas sp. strain in the pure water control. Collectively, these data suggest that interactions between abiotic factors and microbes of the larval environment can help shape mosquito populations' success.