One of the most devastating wheat diseases is stripe rust of wheat caused by the fungal pathogen Puccinia striiformis f. sp. tritici (Pst). In the United States (U.S.), where Pst asexually reproduces, new pathotypes emerge due to events such as mutations within the resident population or through the introduction of exotic populations. The goal of our study was to use a field-transcriptomic approach to evaluate the population structure, evolutionary history, and effector diversity of Pst within the U.S. by determining the genetic diversity of Pst and comparing these results to older U.S. isolates and European isolates. During the 2017 growing season, 25 Pst-infected wheat leaves were collected from fields and compared to 20 Pst transcriptomes from northern Europe (identified in 2013 to 2017) and three additional older U.S. isolates. Our results show the isolates fell into three clusters, with the U.S. samples clustering together in one group regardless of year, and the European samples clustering into two separate groups. These results suggest that recently emergent European races have not been introduced to the U.S. to date, but rather the U.S. diversity may be caused by mutation and adaption within the resident population. The gene expression variability seen within the U.S. population occurs mainly in candidate effectors, which indicates the presence of potentially important genes for distinguishing between U.S. subpopulations.