ABSTRACT Little is known about local adaptation to temperature in bacterial pathogen populations in nature. For plant‐pathogenic bacteria, local thermal adaptation may influence the evolution of virulence, which has strong implications for disease management and mitigation. Xylella fastidiosa ( Xf ) is an insect‐transmitted bacterial pathogen that infects over 700 plant species globally and causes Pierce's disease of grapevines. Here, we compared in vitro growth and in planta virulence of multiple strains from two genetically distinct Xf populations from California regions having either a colder climate (Hopland) or warmer climate (Bakersfield). Xf strains from a warmer climate grew faster than cold‐climate strains under suboptimal (20°C) temperatures, suggesting a lower thermal optimum. In reciprocal field experiments, infections of plants by Xf strains from a colder climate were more likely to survive the winter. After a mild winter in Bakersfield (warmer climate), there were severe symptoms and some vine mortality the following growing season in vines infected with the non‐local, cold‐climate (Hopland) strains, pointing to a potential trade‐off between virulence and transmission due to vine mortality. Our data suggest that Xf populations in CA are locally adapted to temperature, with cold‐climate strains exhibiting hypervirulence when transplanted to warmer climates, whereas warm‐climate strains survive at lower rates when transplanted to colder climates. Thus, local thermal adaptation in bacterial pathogens may influence the optimum virulence phenotype across the landscape.