An understanding of the selective forces leading to evolution of insecticide resistance (IR) is needed to mitigate its threat to malaria vector control. Anopheles albimanus, the main coastal malaria vector in Latin America, shows resistance to various insecticides, including organophosphates (OPs). Following evidence of endosymbiont-mediated IR in agricultural pests, and the identification of OP resistance in An. albimanus, we hypothesized that bacteria may be contributing to insecticide degradation in resistant mosquitoes. To test this, whole metagenome sequencing was used to characterize the microbiota and its functions in Peruvian An. albimanus with differing fenitrothion resistance profiles (resistant, FEN_ Res; susceptible, FEN_Sus). Results showed higher (p<0.01) proportions of OP-degrading bacteria in FEN_Res compared to FEN_Sus, and nine enriched (p<0.05) microbial xenobiotic degradation pathways in FEN_Res. Predominant bacterial species associated with these pathways in FEN_Res were; Klebsiella pneumoniae (81.2%), Acinetobacter baumannii (4.2%), A. pittii (1.6%), and Enterobacter cloacae (0.7%), all known to degrade OPs. The proportion (%) of bacterial enzyme classes involved in these pathways in FEN_Res & FEN_Sus were, hydrolases: 20.1 & 16.3, transferases: 17.8 & 17.9, oxidoreductases: 19.6 & 22.9, lyases: 6.9 & 6.7, isomerases: 0.4 & 0.7, and others: 12.6 & 11.6. At p<0.05 and a difference in proportion between FEN_Res & FEN_Sus (Diff) ≥0.2%, hydrolases, the most enriched enzyme class in FEN_Res, comprised: carboxymethylenebutenolidase (Diff 1.70%), gluconolactonase (Diff 1.46%), alkaline phosphatase (Diff 0.51%), and acid phosphatase (Diff 0.41%) in comparison to FEN_Sus. These results show differential microbial functional profiles between FEN_Res & FEN_Sus, with significant enrichment of hydrolases - the principal class of enzymes involved in biodegradation of OPs - in FEN_Res. Our findings provide novel insights into IR mechanisms that should be considered in the development of new IR monitoring and management tools.