Given the vast quantity of oil and gas input to the marine environment annually, hydrocarbon degradation by marine microorganisms is an essential ecosystem service. Linkages between taxonomy and hydrocarbon degradation capabilities are largely based on cultivation studies, leaving a knowledge gap regarding the intrinsic ability of uncultured marine microbes to degrade hydrocarbons. To address this knowledge gap, metagenomic sequence data from the Deepwater Horizon (DWH) oil spill deep-sea plume was assembled to which metagenomic and metatranscriptomic reads were mapped. Assembly and binning produced new DWH metagenome assembled genomes that were evaluated along with their close relatives, all of which are from the marine environment (38 total). These analyses revealed globally distributed hydrocarbon degrading microbes with clade specific substrate degradation potentials that have not been reported previously. For example, methane oxidation capabilities were identified in all Cycloclasticus. Further, all Bermanella encoded and expressed genes for non-gaseous n-alkane degradation; however, DWH Bermanella encoded alkane hydroxylase, not alkane 1-monooxygenase. All but one previously unrecognized DWH plume members in the SAR324 and UBA11654 coded for aromatic hydrocarbon degradation. In contrast, Colwellia were diverse in the hydrocarbon substrates they could degrade. All clades encoded nutrient acquisition strategies and response to cold temperatures, while sensory and acquisition capabilities were clade specific. These novel insights regarding hydrocarbon degradation by uncultured planktonic microbes provided missing data, allowing for better prediction of the fate of oil and gas when hydrocarbons are input to the ocean, leading to a greater understanding of the ecological consequences to the marine environment.