The release of 700 million liters of oil into the Gulf of Mexico over a few months in 2010 produced dramatic changes in the microbial ecology of the water and sediment. Previous studies have examined the phylogeny and function of these changes, but until now a fundamental examination of the extant hydrocarbon metabolisms that supported these changes had not been performed. Here, we reconstructed the genomes of 57 widespread uncultivated bacteria from post spill sediments, and recovered their gene expression pattern across the seafloor. These genomes comprised a common collection of bacteria that were highly enriched in heavily affected sediments around the wellhead. While rare in distal sediments, some members were still detectable at sites up to 60 km away. Many of these genomes exhibited phylogenetic clustering indicative of common trait selection by the environment, and within half we identified 264 genes associated with hydrocarbon degradation. Observed alkane degradation ability was near ubiquitous among candidate hydrocarbon degraders, while just 3 harbored elaborate gene inventories for the degradation of alkanes and (poly)aromatic hydrocarbons. Differential gene expression profiles revealed a spill-promoted microbial sulfur cycle alongside gene up-regulation associated with polyaromatic hydrocarbon degradation. Gene expression associated with alkane degradation was widespread, although active alkane degrader identities changed along the pollution gradient. The resulting analysis suggests a broad metabolic capacity to respond to oil exists across a large array of usually rare bacteria.