Some species are so linked to specific environments that their habitat association almost becomes a species-defining character and is used by managers and policymakers to direct their conservation. The American lobster Homarus americanus is among the most valuable fisheries species in North America and among the best studied benthic marine invertebrates in the world. Its populations and habitats have been studied and detailed in publications for over 35 yr. This lobster species was known to dwell in shelters, and their populations had historically been concentrated in shelter-providing boulder habitat. Our study revisited 20 long-term monitored sites at 10 m depth along more than 320 km of the Gulf of Maine. Surprisingly, we recorded fundamental changes in lobster abundance, habitat use, and distribution. Specifically, lobster population densities declined overall and occupancy in boulder habitats declined 60%, while densities on featureless ledge and sediment habitats increased 633 and 280%, respectively, from 2000 to 2019. Lobster rock shelter occupancy declined in recent years, but average body size increased, due in part to declines in smaller size classes. These demographic changes may result from both reduced recruitment and intraspecific competition resulting from the lower population densities. Habitat changes at our monitored sites included declines in kelp abundance, increases in diminutive algal turfs, and nearly 3°C warming of benthic water temperature in July (1995-2021), some of which may have contributed indirectly to those shifts. While these changes in shallow water habitat and demography have implications for the lobster fishery and stock assessments, it also illustrates previously undescribed behavioral plasticity.