Marine methane (CH₄) seeps are dynamic biogeochemical systems that regulate carbon and sustain high-biomass communities through microbial CH₄oxidation. While most CH₄ is consumed anaerobically in sediments, a fraction escapes into the water column, where aerobic methanotrophs act as a biological filter limiting atmospheric flux. However, the spatial extent of CH₄ influence beyond active seep zones remains poorly constrained, with implications for deep-sea food webs and carbon cycling. We investigated microbial CH₄turnover and methanotroph distribution across three seep sites on the Southern California margin (Del Mar (1020 m), Santa Monica Mound (800 m), and Lasuen Knoll (400 m)) focusing on extent of horizontal transport, presence of vertical gradients, and oxygen controls. Using radiotracer (³H-CH₄) incubations, CH₄concentration profiles, 16S rRNA gene sequencing, and particulate methane monooxygenase (pmoA) gene quantification, we characterized CH₄-fueled processes along vertical and lateral transects, including near-bottom waters sampled via HOV <em>Alvin</em>. CH₄oxidation was active both within seep plumes and in off-seep waters extending hundreds of meters from the source, with maximum rates reaching 454 nmol L⁻&sup1; d⁻&sup1; in a CH₄-rich bubble plume. Methanotrophic communities showed vertical structuring, with higher diversity near the seafloor. pmoA gene abundances remained consistent across seep and seep-adjacent environments, indicating widespread oxidation potential. Environmental controls were site-specific: oxidation correlated positively with CH₄and negatively with oxygen at some sites, whereas oxygen enhanced oxidation at others. These findings support an expanded &ldquo;methanosphere,&rdquo; in which CH₄-driven microbial processes extend beyond seep boundaries, linking local seep activity to broader deep-sea biogeochemical dynamics.