Bioremediation provides an environmentally sound solution for hydrocarbon removal. Although bioremediation under anoxic conditions is slow, it can be coupled with methanogenesis and is suitable for energy recovery. By altering conditions and supplementing alternative terminal electron acceptors to the system to induce syntrophic partners of the methanogens, this process can be enhanced. In this study, we investigated a hydrocarbon-degrading microbial community derived from chronically contaminated soil. Various hydrocarbon mixtures were used during our experiments in the presence of different electron acceptors. In addition, we performed whole metagenome sequencing to identify the main actors of hydrocarbon biodegradation in the samples. Our results showed that the addition of ferric ions or sulphate increased the methane yield. Furthermore, the addition of CO, ferric ion or sulphate enhanced the biodegradation of alkanes. A significant increase in biodegradation was observed in the presence of ferric ions or sulphate in the case of all aromatic components, while naphthalene and phenanthrene degradation was also enhanced by CO. Metagenome analysis revealed that Cellulomonas sp. is the most abundant in the presence of alkanes, while Ruminococcus and Faecalibacterium spp. are prevalent in aromatics-supplemented samples. From the recovery of 25 genomes, it was concluded that the main pathway of hydrocarbon activation was fumarate addition in both Cellulomonas, Ruminococcus and Faecalibacterium. Chloroflexota bacteria can utilise the central metabolites of aromatics biodegradation via ATP-independent benzoyl-CoA reduction. KEY POINTS: • Methanogenesis and hydrocarbon biodegradation were enhanced by Fe or SO4 • Cellulomonas, Ruminococcus and Faecalibacterium can be candidates for the main hydrocarbon degraders • Chloroflexota bacteria can utilise the central metabolites of aromatics degradation.