Methanogenic communities that degrade alkanes have been reported. However, little is known about the key players involved in the process. Methanogenic hexadecane-degrading consortia were enriched from an oilfield (Shengli, China). The microbial dynamics during the transfer incubations were monitored using terminal restriction fragment length polymorphism (T-RFLP) fingerprinting of 16S rRNA genes in combination with cloning and sequencing. The archaeal community shifted from a predominance of aceticlastic Methanosaeta during early cultivation to a substantial increase in hydrogenotrophic Methanoculleus in the highly enriched culture. Bacterial T-RFs 161 and 164 bp were consistently detected during the incubation and became dominant in the highly enriched culture. T-RF 161 bp primarily represented uncultured Waste Water of Evry 1 bacterium, which was possibly associated with Candidatus Cloacamonas acidaminovorans (99.7% sequence similarity). T-RF 164 bp could be assigned to both Thermotogaceae, with the closest relative being Candidatus Mesotoga sulfurreducens (similarity of 97%) and Syntrophaceae, with Smithella propionica as the closest relative (similarity of 96–97%). These bacterial lineages were potentially capable of syntrophic interactions with methanogen partners during hexadecane degradation. Partial assA genes (encoding the α-subunit of alkylsuccinate synthase) were also detected, implying that the mechanism of fumarate addition may function in the hexadecane activation.