Big-bracted dogwoods are popular ornamental trees known for their beautiful spring blooms with showy bracts and four-season appeal. The two most widely grown species are Cornus florida and Cornus kousa, native to Eastern North America and East Asia. Despite their horticultural prominence, there is little information available regarding genetic diversity, population structure, relatedness, and subspecies origins of dogwood cultivars. In this study, 313 cultivars, wild-collected plants, and Rutgers University breeding selections, focusing on C. florida, C. kousa, and interspecific hybrids, were genotyped using restriction-site associated DNA sequencing (RADseq) generating thousands of single nucleotide polymorphism (SNP) and insertion deletion (Indel) markers. The research results showed high genetic diversity among C. florida and C. kousa wild-collected plants and cultivars. For C. florida, pink-bracted plants formed a distinct clade from those with white-bracts with the Mexican C. florida ssp. urbiniana forming an outgroup. For C. kousa, Chinese-collected plants (ssp. chinensis) were a distinct subspecies with clear separation from Japanese and Korean accessions (ssp. kousa) and cultivars were designated as ssp. chinensis, ssp. kousa, or ssp. hybrid. Using this information, a Kompetitive allele specific PCR (KASP) assay genotyping panel was designed to determine C. kousa trees’ subspecies makeup. Results revealed many cases of genetically identical cultivars being sold under different names, especially for pink-bracted cultivars of both species. Additionally, reported parent-progeny relationships were evaluated and either validated or discredited. Finally, the hybrid germplasm analysis validated pedigrees of interspecific F1 hybrids and found many of the recent Rutgers breeding selections contain small regions of pacific dogwood (C. nuttallii) DNA introgressed into C. kousa backgrounds. This diversity study elucidates origins, diversity, and relationships of a large population of big-bracted dogwoods. The results can inform plant breeders, arboreta, and the ornamental plant industry, as most modern cultivars and popular historic cultivars are represented.