In light of the declining global malaria burden attained largely due to insecticides, a deeper understanding of the factors driving insecticide resistance is needed to mitigate its growing threat to malaria vector control programs. Following evidence of microbiota-mediated insecticide resistance in agricultural pests, we undertook a comparative study of the microbiota in mosquitoes of differing insecticide resistance status. The microbiota of wild-caught Anopheles albimanus, an important Latin American malaria vector, that were resistant (FEN-Res) or susceptible (FEN-Sus) to the organophosphate (OP) insecticide fenitrothion were characterized and compared using whole metagenome sequencing. Results showed differing composition of the microbiota and its functions between FEN-Res and FEN-Sus, with significant enrichment of OP-degrading bacteria and enzymes in FEN-Res compared to FEN-Sus. Lower bacterial diversity was observed in FEN-Res compared to FEN-Sus, suggesting the enrichment of bacterial taxa with a competitive advantage in response to insecticide selection pressure. We report and characterize for the first time whole metagenomes of An. albimanus, revealing associations between the microbiota and phenotypic resistance to the insecticide fenitrothion. This study lays the groundwork for further investigation of the role of the mosquito microbiota in insecticide resistance.