Bacterial biodegradation is a significant contributor to remineralization of polycyclic aromatic hydrocarbons (PAHs), which are a component of crude oil and marine diesel as well as byproducts of partial combustion chronically introduced into seawater via atmospheric deposition. The Deepwater Horizon oil spill demonstrated the speed in which a seed PAH-degrading community maintained by low chronic inputs can respond to an acute pollution. We investigated various aspects of this seed community in a chronically polluted site, the Port of Los Angeles, using high-resolution stable isotope probing with naphthalene, deep-sequenced metagenomes and carbon incorporation rate measurements at the port and in two sites further into the San Pedro Channel. We show a potential succession of PAH degradation from a diverse community which may rely on a consortium in order to achieve full detoxification towards specialized taxa, and discuss additional metabolic requirements those specializers may have. We also highlight a contradiction between PAH-degrading capabilities within assembled genomes, raw reads and incorporation rates which may be due to degradation of naphthalene by non-traditional enzymes. The results of this study emphasize the ability of the local seed community to respond directly to PAH inputs independently of a labile-hydrocarbon degrading succession, as occurred during the Deepwater Horizon disaster, focusing on the more recalcitrant component of hydrocarbon pollution.