<p>Epoxiconazole (EPO) and fludioxonil (FLU) are fluorinated fungicides known for their extremely high environmental persistence and significant ecotoxicological impact. Given their decades-old use in the agrochemical sector, EPO and FLU became frequent pollutants of terrestrial and aquatic ecosystems. And yet, not much is known regarding how these pesticides biodegrade in the natural environment or how to develop suitable bioremediation approaches capable of tackling their inherent recalcitrance. As such, this work focused on providing new insights into the bacterial degradation of EPO and FLU, by surveying the catabolic activity of a previously obtained EPO-enriched bacterial consortium through chemical and metaproteogenomic analyses guided by different metabolic modelling tools. The bacterial consortium was capable of extensively degrading EPO and FLU in 21 days, with fungicide removals of over 90% and defluorination efficiencies of up to 80%, but none of the subproducts predicted in silico were identified for either pesticide. Despite this, the combination of metabolic modelling tools and metaproteogenomic surveys suggested that EPO and FLU were first attacked in their N-heterocyclic moieties and that the targets of defluorination were the resulting aromatic fluorinated intermediates. This catabolic cascade is consistent with the experimental data gathered in this study and with the existing literature on this topic. Also, the degrading consortium remained stable at the taxonomical and functional levels, highlighting its catabolic plasticity in biodegrading and defluorinating two chemically distinct fluorinated compounds. This work offers a conceptual framework with novel observations that can guide future efforts to further elucidate the pathways of microbial transformation of these pesticides, ultimately contributing to better environmental risk management practices for these pollutants.</p>