Several explanations have been posited for how the plague bacterium (Yersinia pestis) reemerges during sylvatic cycles within the same foci over many years, and often without direct evidence of host die-offs. One prevalent view is that transmission-optimized Y. pestis bacteria, exhibiting epizootic/enzootic behavior, almost continually replicate and survive through repeated, linked, host-centered propagation events. These bacteria, we will refer to as “r-pestis” type ecotype(s), represent a limited number of phenotypic lineages exhibiting optimal transmissibility and high rates of reproduction. These attributes, it is thought, assure their durability through time. For continuous r-pestis type expansions to be successful, adequate numbers of fleas and hosts must become infected to produce massive numbers of bacteria. In the process, host and flea numbers decline as they succumb to plague. Here we hypothesize that r-pestis population expansions seed the environment and confront a unique, highly competitive local milieu, where natural selection favors new ecotypes that incorporate a range of emergent adaptive survival strategies. These newly adapted survivors we recognize as a range of “K-pestis” ecotypes with greater durability and lower reproduction rates. These emergent K-pestis forms may arise in succession or coexist for varying periods of time with r-pestis ecotypes, and with other K-pestis ecotypes. Among K-pestis ecotypes, we hypothesize that through adaptive radiations, some persist within flea life stages, soil, organic waste, amoebae, plants, carcasses, hosts, or within niches yet to be characterized. In some settings, after a long quiet period, when favorable, K-pestis bacteria may trigger a singular event where an r-pestis transmission stream emerges precipitating another enzootic/epizootic progression. If this hypothesis withstands rigorous testing, then Y. pestis might represent an even more formidable, enduring, and adaptable foe, where unforeseen local events could trigger new epidemic and epizootic/enzootic events threatening humans and populations of other mammals, including those of conservation concern.