The emergence of high-throughput, high-density genotyping methods combined with increasingly powerful computing systems has created opportunities to further discover and exploit the genes controlling agronomic performance in elite maize breeding populations. Understanding the genetic basis of population structure in an elite set of materials is an essential step in this genetic discovery process. This paper presents a genotype-based population analysis of all maize inbreds whose Plant Variety Protection certificates had expired as of the end of 2013 (283 inbreds) as well as 66 public founder inbreds. The results provide accurate population structure information and allow for important inferences in context of the historical development of North American elite commercial maize germplasm. Genotypic data was obtained via genotyping-by-sequencing on 349 inbreds. After filtering for missing data, 77,314 high-quality markers remained. The remaining missing data (average per individual was 6.22 percent) was fully imputed at an accuracy of 83 percent. Calculation of linkage disequilibrium revealed that the average r2 of 0.20 occurs at approximately 1.1 Kb. Results of population genetics analyses agree with previously published studies that divide North American maize germplasm into three heterotic groups: Stiff Stalk, Non-Stiff Stalk, and Iodent. Principal component analysis shows that population differentiation is indeed very complex and present at many levels, yet confirms that division into three main sub-groups is optimal for population description. Clustering based on Nei's genetic distance provides an additional empirical representation of the three main heterotic groups. Overall fixation index (FST), indicating the degree of genetic divergence between the three main heterotic groups, was 0.1361. Understanding the genetic relationships and population differentiation of elite germplasm may help breeders to maintain and potentially increase the rate of genetic gain, resulting in higher overall agronomic performance.