The ecological success of widespread species is attributed to an ability to generalize across diverse habitats, a so-called “jack of all trades” scenario. However, this assumption ignores the potential for local specialization, an alternative scenario whereby spatial variation in natural selection generates habitat-specific adaptive landscapes. Despite a growing recognition of spatial variation in selection in nature, and the inevitable exploitation of distinct habitat types across an extensive geographic range, attention to this hypothesis has been lacking for widespread taxa. We test this hypothesis using data from four populations of a widespread species drawing from two distinct habitat types (tree- and boulder-dominated, respectively). Specifically, we compare major physiological traits of male and female lizards by habitat type and then estimate the form of natural selection on those traits for each sex in each habitat (i.e., their adaptive landscapes). We detected significant differences in morphology and performance across habitats that mirror interspecific patterns. Importantly, patterns of linear and non-linear selection on these traits were habitat-specific for both sexes, indicating a clear but underappreciated capacity for local specialization. Our findings directly challenge assumptions of habitat generalism in widespread taxa, and instead reveal a novel role for adaptive diversification in driving their ecological success.