Altered thermal regimes under climate change may influence host-parasite interactions and invasive species, both potentially impacting valuable ecosystem services. There is considerable interest in how parasite life cycle rates, growth, and impacts on hosts will change under altered environmental temperatures. Likewise, transformed thermal regimes may reduce natural resistance and barriers preventing establishment of invasive species or alter the range and impacts of established exotic species. The Laurentian Great Lakes are some of the most invaded ecosystems and have been profoundly shaped by exotic species. Invasion by the parasitic sea lamprey (Petromyzon marinus) contributed to major declines in many Great Lakes fish populations. In Lake Superior, substantial progress has been made towards controlling invasive sea lamprey and rehabilitating native fish populations. Surface water temperatures in Lake Superior have been increasing rapidly since 1980 presenting a new challenge for management. Here we test how thermal changes in Lake Superior have impacted the feeding and growth of the parasitic sea lamprey. Sea lamprey have increased in size corresponding with longer durations of thermal habitat (i.e., longer growing seasons) for their preferred hosts. To compare regional differences in sea lamprey feeding and growth rates, we used a bioenergetics model with temperature estimates from a lake-wide hydrodynamic model hindcast from 1979–2006. Spatial differences in patterns of warming across the lake result in regionally different predictions for increases in sea lamprey feeding rates and size. These predictions were matched by data from adult sea lamprey spawning in streams draining into these different thermal regions. Larger sea lampreys will be more fecund and have increased feeding rates, thus increasing mortality among host fishes. Resource management should consider these climate driven regional impacts when allocating resources to sea lamprey control efforts. Under new and evolving thermal regimes, successful management systems may need to be restructured for changing phenology, growth, and shifts in host-parasite systems towards greater impacts on host populations.