Atmospheric mercury (Hg) deposition has been declining in North America but remains the dominant delivery mechanism to the Great Lakes. The Lakes are highly efficient at bioaccumulating methylmercury, making the fish excellent sentinels for tracking shifts in atmospheric Hg deposition. Invasive mussels have altered biogeochemical processes, prey populations and fish dietary strategies asynchronously and to varied extents across the lower four lakes, impacting fish Hg exposure. To test if fish are adapting to new biogeochemical conditions, we analyzed a 40 year fish archive for carbon and nitrogen isotope ratios and amino acid-specific nitrogen isotope ratios. To assess Hg sources, we measured Hg isotope ratios. We reconstructed and compared energetic pathways that impact fish Hg concentrations to Hg-source trends. We found fish-Hg concentrations are declining but not monotonically due to ecological disturbances. Fish-Hg isotope values, unimpacted by ecological disturbance, confirm that sources of bioaccumulated Hg shift contemporaneously with changes in atmospheric Hg concentrations. Across Lakes, the degree of responsiveness to changes in atmospheric Hg concentrations mirrors the proportion of atmospheric-delivered Hg we previously modeled. Changes in both fish concentrations and fish isotope values outpace paleolimnetic reconstructions suggesting declines in atmospheric Hg concentrations impact fish Hg more than sediment.