Carbon flow in a model methanogenic consortium capable of hydrocarbon degradation was investigated using a combination of stable isotope fractionation, protein-based stable isotope probing, and metaproteomics. Overall δ¹³C enrichment for methane and CO₂ in the presence and absence of oil suggests that complex microbial interactions occur during methanogenic hydrocarbon mineralization. Specifically, the Δδ¹³C of CO₂ was statistically identical in all incubations irrespective of oil presence, but the Δδ¹³C for methane was greater in the presence of oil compared with fatty acids alone. In addition, carbon from uniformly (¹³C) labelled n-fatty acids was distributed evenly among consortium members in the presence of oil, but used by relatively few community members when provided alone. In all incubations, aceticlastic and hydrogenotrophic methanogens were labelled to an equal extent, suggesting that no pathway is overwhelmingly dominant during methane production by the model consortium. Protein-based stable isotope probing identified key enzymes responsible for methanogenesis from CO₂ and acetate labelled with 78.0 ± 4.4% and 73.3 ± 1.0% ¹³C respectively. Results suggest that acetate was used directly by methanogens in the presence of n-fatty acids alone, and that methanogenesis from CO₂ was a secondary process. Proteins capable of catalysing hydrocarbon activation by addition to fumarate were not found. Collectively, this study demonstrates that significant microbial cooperation is required to recover hydrocarbons as methane.