Summary Large quantities of organic matter are continuously deposited, and (a)biotic gradients intersect in the soil–rhizosphere, where biodegradation contributes to the global cycles of elements. The betaproteobacterial genus Aromatoleum comprises cosmopolitan, facultative denitrifying degradation specialists. Aromatoleum aromaticum. pCyN1 stands out for anaerobically decomposing plant‐derived monoterpenes in addition to monoaromatic hydrocarbons, polar aromatics and aliphatics. The catabolic network's structure and flexibility in A. aromaticum pCyN1 were studied across 34 growth conditions by superimposing proteome profiles onto the manually annotated 4.37 Mbp genome. Strain pCyN1 employs three fundamentally different enzymes for C–H‐bond cleavage at the methyl groups of p‐cymene/4‐ethyltoluene, toluene and p‐cresol respectively. Regulation of degradation modules displayed substrate specificities ranging from narrow (toluene and cyclohexane carboxylate) via medium‐wide (one module shared by p‐cymene, 4‐ethyltoluene, α‐phellandrene, α‐terpinene, γ‐terpinene and limonene) to broad (central benzoyl‐CoA pathway serving 16 aromatic substrates). Remarkably, three variants of ATP‐dependent (class I) benzoyl‐CoA reductase and four different β‐oxidation routes establish a degradation hub that accommodates the substrate diversity. The respiratory system displayed several conspicuous profiles, e.g. the presence of nitrous oxide reductase under oxic and of low‐affinity oxidase under anoxic conditions. Overall, nutritional versatility in conjunction with network regulation endow A. aromaticum pCyN1 with broad adaptability.