Since the discovery of cable bacteria more than a decade ago, these multicellular, filamentous sulfur-oxidizing bacteria have been found in a range of sedimentary environments. However, their abundance, diversity, and activity in continental margin sediments overlain by oxygen-deficient waters at water depths of > 100 m remain poorly known. Here we address this by studying five basins along the coasts of California and Mexico. All sediments are organic carbon rich (2.5 wt %–7.5 wt %) and characterized by active iron and sulfur cycling. Nitrate is present in the bottom water at all sites. Results of fluorescence in situ hybridization (FISH) indicate a low areal abundance of cable bacteria (0.2 to 19 m cm−2) in sediments of the hypoxic San Clemente, Catalina, and San Pedro basins and the anoxic San Blas basin. In the anoxic Soledad basin, in contrast, we found abundant cable bacteria near the sediment surface (129 m cm−2). DNA amplicon sequencing detected cable bacteria reads in sediments of the hypoxic San Pedro basin and the anoxic Soledad and San Blas basins. Phylogenetic analysis indicated that the diversity of the amplicon sequence variants (ASVs) was spread across the Candidatus Electrothrix lineage, including multiple ASVs closely related to Electrothrix gigas, a recently discovered species of giant cable bacteria. Additionally, multiple sequences retrieved from the Soledad and San Blas basins revealed affiliation with a clade sister to Electrothrix, hypothesized as a novel genus, suggesting possible relic or novel adaptations of cable bacteria to these anoxic and nitrogenous environments. The areal abundance of cable bacteria was negatively related to sediment Fe / S ratios, suggesting a control by sulfide availability. However, free sulfide in the porewater was only detected at the anoxic Soledad site. Micro-profiling of pH and electric potential points toward a lack of cable bacteria activity at the time of sampling, possibly due to a limitation by a suitable electron donor and/or acceptor. Periodically enhanced organic matter input and associated sulfate reduction and/or inflows of oxic water could alleviate the deficiency, creating the observed niche for diverse cable bacteria.