Sulfate-dependent anaerobic oxidation of methane (AOM) is the key sedimentary microbial process limiting methane emissions from marine sediments and methane seeps. In this study, we investigate how the presence of low-organic content sediment influences the capacity and efficiency of AOM at Bullseye vent, a gas hydrate-bearing cold seep offshore of Vancouver Island, Canada. The upper 8 m of sediment contains < 0.4 wt% total organic carbon (OC) and primarily consists of glacially-derived material that was deposited 14,900 to 15,900 yrs BP during the retreat of the late Quaternary Cordilleran Ice Sheet. We hypothesize this aged and exceptionally low-OC content sedimentary OM is biologically refractory, thereby limiting degradation of non-methane OM by sulfate reduction and maximizing methane consumption by sulfate-dependent AOM. A radiocarbon-based dissolved inorganic carbon (DIC) isotope mass balance model demonstrates that respired DIC in sediment pore fluids is derived from a fossil carbon source that is devoid of ¹⁴C. A fossil origin for the DIC precludes remineralization of non-fossil OM present within the sulfate zone as a significant contributor to pore water DIC, suggesting that nearly all sulfate is available for anaerobic oxidation of fossil seep methane. Methane flux from the SMT to the sediment water interface in a diffusion-dominated flux region of Bullseye vent was, on average, 96% less than at an OM-rich seep in the Gulf of Mexico with a similar methane flux regime. Evidence for enhanced methane oxidation capacity within OM-poor sediments has implications for assessing how climate-sensitive reservoirs of sedimentary methane (e.g., gas hydrate) will respond to ocean warming, particularly along glacially-influenced mid and high latitude continental margins.