High methylmercury (MeHg) concentrations in Arctic marine biota have been linked to high MeHg uptake driven by shallow MeHg peaks at water depths of 100–300 m in the Arctic Ocean. To understand how the biogeochemical characteristics of each basin affects the distribution of total Hg (THg) and MeHg across the Arctic Ocean, the spatial patterns of THg and MeHg were investigated using data from new transects in the Beaufort Sea (BS) and previously published Arctic Ocean expeditions covering the Canada Basin and Makarov Basin in the Pacific sector, and Amundsen Basin and Nansen Basin in the Atlantic sector. In the BS, the THg concentration in the polar mixed water increased with salinity (r = 0.87, p < 0.01), which was linked to THg transport from the Chukchi Shelf. Transport of Hg from the Chukchi Shelf also drove elevated THg concentrations in the polar mixed water and halocline water in the Canada Basin and Makarov Basin compared to other Arctic basins. The MeHg concentration in the BS was positively correlated with the biological index in the Pacific summer water (r = 0.86, p < 0.01), demonstrating that intrusion of warm and nutrient-rich Pacific water promotes MeHg production in the BS. In line with this result, chlorophyll-a showed a comparable cross-basin trend to that of MeHg, with the highest values in the Nansen Basin. In the halocline water, MeHg concentrations were highest in the Canada Basin likely due to the largest availability of Hg(II). On the contrary, MeHg concentration was highest in the Nansen Basin in the Atlantic water layer, which could be related to the higher seawater temperature and enhanced biological production. The results of this study underscore the critical role of Pacific and Atlantic inflows in modulating the profiles of THg and MeHg in the Arctic Ocean.