Petroleum hydrocarbons are important for their energy value and the environmental concerns they pose when spilled. Methanogenic biodegradation through syntrophy plays an important role in their degradation, with implications for remediation and oil recovery. There is still much to learn about methanogenic biodegradation of recalcitrant hydrocarbons such as paraffinic n-alkanes, or the overall syntrophic metabolism underlying these processes. Here, methanogenic solid and liquid paraffin-degrading enrichments were established, with Smithella identified as the hydrocarbon degrader. Fumarate addition was identified as the putative hydrocarbon activation mechanism through alkylsuccinate synthase gene presence and expression, and factors (biosurfactant production) which affect biodegradation were determined. In addition, gene families related to energy transfer were found to distinguish known and potentially syntrophic environments using metagenomic analysis. This approach was used to determine gene families which may play unknown roles in syntrophy. Together, these studies give key insights into how hydrocarbons are degraded under methanogenic conditions.