Adaptive developmental plasticity occurs when juvenile development changes in response to information about the environment, leading to adult traits that confer superior performance under changing conditions. Adaptive plasticity may underlie the potential for species to invade new habitats by enabling persistence in sub-optimal contexts until there is sufficient time for evolutionary (genetic) adaptation. However, many forms of plasticity are maladaptive, with environmental induction of changed gene expression leading to decreased adult fitness. Moreover, it is not yet clear whether adaptive plasticity confers increased invasive potential in the long run. In two ‘black’ widow spider species (Latrodectus hesperus and the invasive L. hasselti), we used field surveys and pheromone traps to demonstrate the existence of significant spatio-temporal variation in the adult traits (development time, body size, mobility) that confer success in sexual competition under variable environments (population density, proximity of mates, seasonal demography). In the lab, we manipulated juvenile exposure to pheromones or seasonal cues that predict population density and the form of sexual competition, then monitored development, adult phenotypes (morphology, longevity, metabolic rate), and assayed proxies for adult fitness (mobility, reproductive success). We show that species-specific cues triggered changes in development time, and also led to variation in adult traits. Plastic adults (males and females) showed superior performance under the challenges that triggered the plasticity. This work establishes widow spiders as excellent models to investigate adaptive plasticity and suggests comparative analyses across the 30 species in the genus Latrodectus may yield important evolutionary insights into links between invasiveness and plasticity.