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Pestis secunda (1356–1366 CE) is the first of a series of plague outbreaks in Europe that followed the Black Death (1346–1353 CE). Collectively this period is called the Second Pandemic. From a genomic perspective, the majority of post-Black Death strains of Yersinia pestis thus far identified in Europe display diversity accumulated over a period of centuries that form a terminal sub-branch of the Y. pestis phylogeny. It has been debated if these strains arose from local evolution of Y. pestis or if the disease was repeatedly reintroduced from an external source. Plague lineages descended from the pestis secunda, however, are thought to have persisted in non-human reservoirs outside Europe, where they eventually gave rise to the Third Pandemic (19th and 20th centuries). Resolution of competing hypotheses on the origins of the many post-Black Death outbreaks has been hindered in part by the low representation of Y. pestis genomes in archaeological specimens, especially for the pestis secunda. Here we report on five individuals from Germany that were infected with lineages of plague associated with the pestis secunda. For the two genomes of high coverage, one groups within the known diversity of genotypes associated with the pestis secunda, while the second carries an ancestral genotype that places it earlier. Through consideration of historical sources that explore first documentation of the pandemic in today's Central Germany, we argue that these data provide robust evidence to support a post-Black Death evolution of the pathogen within Europe rather than a re-introduction from outside. Additionally, we demonstrate retrievability of Y. pestis DNA in post-cranial remains and highlight the importance of hypothesis-free pathogen screening approaches in evaluations of archaeological samples. Author summary: We present two high-coverage and three low-coverage ancient Y. pestis genomes that represent previously described diversity within a narrow time interval that immediately post-dates the Black Death (the pestis secunda), and a newly identified precursor strain. Viewed in context with recent historical revelations that define the time-span between the end of the Black Death and the emergence of the pestis secunda to a three-year interval, our analysis strongly supports this outbreak, similar to other post-Black Death outbreaks, as having originated from a local source of Y. pestis diversification. [ABSTRACT FROM AUTHOR]