Long-term hydrocarbon pollution is a devious threat to aquatic and marine ecosystems. However, microbial responses to chronic pollution remain poorly understood. Combining genome-centric metagenomic and metatranscriptomic analyses of microbial mat samples that experienced chronic hydrocarbon pollution for more than 80 years, we analyzed the transcriptomic activity of alkane and aromatic hydrocarbon degradation pathways at the population level. Consistent with the fluctuating and stratified redox conditions of the habitat, both aerobic and anaerobic hydrocarbon degradation pathways were expressed by taxonomically and metabolically contrasted lineages including members of Bacteroidiales, Desulfobacteraceae, Pseudomonadales; Alcanivoraceae and Halieaceae populations with (photo)-heterotrophic, sulfur- and organohalide-based metabolisms, providing evidence for the co-occurrence and activity of aerobic and anaerobic hydrocarbon degradation pathways in shallow marine microbial mats. In addition, our results suggest that aerobic alkane degradation in long-term pollution involved bacterial families that are naturally widely distributed in marine habitats, but hydrocarbon concentration and composition were found to be a strong structuring factor of their intrafamily diversity and transcriptomic activities.