To constrain the fluxes of methane (CH4) in the water column above the accretionary wedge along the Cascadia continental margin, we measured methane and its stable carbon isotope signature (δ13C-CH4). The studies focused on Hydrate Ridge (HR), where venting occurs in the presence of gas-hydrate-bearing sediments. The vent CH4 has a light δ13C-CH4 biogenic signature (−63 to −66‰ PDB) and forms thin zones of elevated methane concentrations several tens of meters above the ocean floor in the overlying water column. These concentrations, ranging up to 4400 nmol L−1, vary by 3 orders of magnitude over periods of only a few hours. The poleward undercurrent of the California Current system rapidly dilutes the vent methane and distributes it widely within the gas hydrate stability zone (GHSZ). Above 480 m water depth, the methane budget is dominated by isotopically heavier CH4 from the shelf and upper slope, where mixtures of various local biogenic and thermogenic methane sources were detected (−56 to −28‰ PDB). The distribution of dissolved methane in the working area can be represented by mixtures of methane from the two primary source regions with an isotopically heavy background component (−25 to −6‰ PDB). Methane oxidation rates of 0.09 to 4.1% per day are small in comparison to the timescales of advection. This highly variable physical regime precludes a simple characterization and tracing of “downcurrent” plumes. However, methane inventories and current measurements suggest a methane flux of approximately 3 × 104 mol h−1 for the working area (1230 km2), and this is dominated by the shallower sources. We estimate that the combined vent sites on HR produce 0.6 × 104 mol h−1, and this is primarily released in the gas phase rather than dissolved within fluid seeps. There is no evidence that significant amounts of this methane are released to the atmosphere locally.