The reconstruction of the evolutionary histories of pathogen populations in space and time has greatly improved our understanding of their epidemiology. However, analyses are usually restricted to the non-recombining genomic regions and, thus, fail to inform on the dynamics of the accessory genome. Yet, horizontal gene transfer is of striking importance to the evolution of bacteria as it can redistribute phenotypically important genes. For bacterial pathogens, those include resistance to antimicrobial compounds and virulence factors. Understanding the gene turnover in genomes at microevolutionary scales is key to apprehend the pace of this evolutionary process. Here we addressed this question for the epidemic lineage of a major bacterial plant pathogen, relying on a dense geographic sampling spanning 39 years of evolution. Gene turnover rate exceeded SNP mutation rates by three orders of magnitude. Accessory genes were preferentially plasmid-encoded, but we evidenced a highly plastic chromosomal region hosting ecologically important genes such as transcription activator-like effectors. We argue that turnover of accessory genes provides a potent evolutionary force in monomorphic bacteria, and exemplify this statement retracing the history of a mobile element conferring resistance to copper compounds widely used for the management of plant bacterial pathogens.