Abstract
Summary Xylella fastidiosa subsp. fastidiosa causes Pierce's disease of grapevine (PD) and has been present in California for over a century. A singly introduced genotype spread across the state causing large outbreaks and damaging the grapevine industry. This study presents 122 X . fastidiosa subsp. fastidiosa genomes from symptomatic grapevines, and explores pathogen genetic diversity associated with PD in California. A total of 5218 single‐nucleotide polymorphisms (SNPs) were found in the dataset. Strong population genetic structure was found; isolates split into five genetic clusters divided into two lineages. The core/soft‐core genome constituted 41.2% of the total genome, emphasizing the high genetic variability of X . fastidiosa genomes. An ecological niche model was performed to estimate the environmental niche of the pathogen within California and to identify key climatic factors involved in dispersal. A landscape genomic approach was undertaken aiming to link local adaptation to climatic factors. A total of 18 non‐synonymous polymorphisms found to be under selective pressures were correlated with at least one environmental variable highlighting the role of temperature, precipitation and elevation on X . fastidiosa adaptation to grapevines in California. Finally, the contribution to virulence of three of the genes under positive selective pressure and of one recombinant gene was studied by reverse genetics.