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Large proglacial lakes could have been a significant methane source during the last deglaciation. Today, proglacial lakes are small and mostly limited in the northern hemisphere to the margins of ice sheets in Greenland, Alaska, and Canada, but much larger proglacial lakes collectively flooded millions of square kilometers in the northern hemisphere over the last deglacial period. We synthesize new and existing methane flux measurements from modern proglacial lakes in Alaska and Greenland and use these data together with reconstructed lake area and bathymetry, new paleorecords of sediment organic geochemistry, carbon accumulation, and other proxies to broadly constrain the possible deglacial methane dynamics of a single large North American proglacial lake, Lake Agassiz. While large influxes of glaciogenic material contributed to rapid organic carbon burial during initial lakes phases, limited bioavailability of this carbon is suggested by its likely subglacial origin and prior microbial processing. Water depths of >20 m across 37–90% of the lake area facilitating significant oxidation of methane within the water column further limited emissions. Later phases of lake lowering and subsequent re-expansion into shallow aquatic and subaerial environments provided the most significant opportunity for methane production according to our estimates. We found that Lake Agassiz was likely a small source [0.4–2.7 Tg yr−1 mean (0.1–9.9 Tg yr−1 95% CI)] of methane during the last deglaciation on par with emissions from modern wildfires. Although poor constraints of past global proglacial lake areas and morphologies currently prevent extrapolation of our results, we suggest that these systems were likely an additional source of methane during the last deglacial transition that require further study.