Sediments underlying marine hypoxias are huge sinks of unreacted complex organic matter, where despite acute O2-limitation aerobic bacterial communities thrive, and near-complete depletion of organic carbon takes place within a few meters below the seafloor. However, little knowledge exists about how aerobic chemoorganotrophs survive in these sulfidic ecosystems, and what may be their potentials for degrading complex carbon compounds. To elucidate these questions, we isolated and characterized a number of aerobic bacterial chemoorganoheterotrophs from across a ∼3-m sediment horizon underlying the perennial hypoxia of the eastern Arabian Sea. High levels of sequence correspondence between the isolates’ genomes and the habitat’s metagenomes and metatranscriptomes illustrated that the strains were widespread and active across the sediment cores explored. The isolates could catabolize several complex organic compounds of marine and terrestrial origins, via aerobic respiration at high as well as low O2concentrations. Some of them could also grow anaerobically on yeast extract or acetate by reducing nitrate and/or nitrite. Fermentation did not support growth in any of the strains, but enabled all of them to maintain a fraction of the cell population amidst prolonged anoxia. Under extreme oligotrophy, robust growth followed by protracted stationary phase was observed for all the isolates at low cell density, irrespective of whether O2was high or low. While metabolic deceleration was apparently central to the strains’ adaptation to dwindling organic carbon, O2-limitation could be potentially surmounted via supplies from known producers of biogenic O2, such asNitrosopumilusspecies, which had copious footprints in the habitat’s metagenomes.