Since the first descriptions of Pseudomonas syringae as a plant-associated bacterium, the vision of its ecology has moved away from ubiquitous epiphytic plant pathogen to multi-faceted bacterium sans frontières in fresh water and other ecosystems linked to the water cycle. Discovery of the aquatic facet of its ecology has led to a vision of its life history that integrates spatial and temporal scales spanning billions of years and traversing catchment basins, continents and the planet, and that confronts the implication of roles that are potentially conflicting for agriculture – as a plant pathogen and as an actor in processes leading to rain and snowfall. This new ecological perspective has also yielded insight into epidemiological phenomena linked to disease emergence. It sets the stage for the integration of more comprehensive contexts of ecology and evolutionary history into comparative genomic analyses to elucidate how P. syringae subverts attack and defense responses of the cohabitants of the diverse environments it occupies. Here we will present our vision of the evolving story of the ecology and biology of P. syringae and we will speculate on how this story will continue to evolve in the future.