Significance Carbapenem-resistant Enterobacteriaceae (CRE) are an urgent threat: as an increasing cause of disease and as the staging ground for resistance to “last line” drugs. Thus, we must understand how CRE evolve, diversify, and spread and especially the potential for asymptomatic transmission without outbreaks. Our broad sample of species and genetic determinants that defined four hospital CRE communities over 16 mo revealed a significant degree of CRE diversity, with little evidence for clonal spread but extensive movement of resistance determinants. We provide evidence for considerable asymptomatic carriage and unrecognizable mechanisms of carbapenem resistance that, together, indicate continued innovation by these organisms to thwart the action of this important class of antibiotics and underscore the need for continued surveillance of CRE.