<p>Understanding local adaptation of phytopathogens has significant practical and economic implications. The opportunistic pathogen <i>Pseudomonas syringae</i> exemplifies this challenge, causing regular epidemics in diverse host plants. Many pathogenic microbes, including <i>P. syringae</i>, are divided into intraspecific lineages, or pathovars, based on their host-of-isolation. However, whether pathovar classifications reflect adaptation of the pathogen to the host (local adaptation) or a competitive advantage of the pathogen in the host (local dominance), often goes untested. In this study, we performed <i>in vitro</i> growth assays and factorial controlled infections to test whether a suite of five <i>P. syringae</i> pathovars are locally adapted to, and/or locally dominant in, their hosts-of-isolation. We found evidence of local adaptation in three of five pathogens, only one of which was also locally dominant. Several strains performed as well or better than the locally adapted strain in that strain’s host-of-isolation, consistent with cost-free generalism. Thus, pathovar designations do not reliably delineate pathogenic phenotypes. Moreover, we found that <i>in vitro</i> growth was not predictive of <i>in planta</i> growth. To contextualize phenotypes, we compared pathogen gene content, identifying unique phytotoxins, secreted effectors, and general virulence factors. In all, we found that local adaptation is common but not universal, and that locally adapted strains are not necessarily constrained from performing competitively in multiple hosts. Thus, neither host-of-isolation nor <i>in vitro</i> performance is reliable for strain classification. Our findings highlight the vast intraspecific variation in <i>P. syringae</i>, and the coexistence of multiple successful adaptive strategies.</p>