The ubiquitous marine bacterium Vibrio parahaemolyticus is a leading cause of illness associated with seafood consumption. The emergence of two genetically distinct ecotypes (ST3 and ST36) has led to an alarming increase in the size and frequency of disease outbreaks. We conducted a genomic comparison of 30 V. parahaemolyticus genomes that represent a diverse collection of 15 genetically distinct ecotypes, including newly sequenced representatives of ST3 and ST36, isolated from both clinical and environmental sources. A multistep evolutionary analysis showed that genes associated with sensing and responding to environmental stimuli have evolved under positive selection, identifying examples of convergent evolution between ST3 and ST36. A comparison of predicted proteomes indicated that ST3 and ST36 ecotypes laterally acquired tens of novel genes associated with a variety of functions including dormancy, homeostasis and membrane transport. Genes identified in this study play an apparent role in environmental fitness and may confer cross protection against stressors encountered in the human host. Together, these results show the evolution of stress response is an important genetic mechanism correlated with the recent emergence of the ST3 and ST36 ecotypes.