Rose rosette virus (RRV), also known as Emaravirus rosae, causes Rose rosette disease (RRD) of roses across the United States. Over the past few decades, it has severely impacted the rose industry and local landscapes, diminishing the beauty of rose gardens. In Oklahoma, RRV has completely wiped out local rose gardens. Understanding the diversity of the virus is crucial for developing effective diagnostic tools and improving management strategies. Previous studies have indicated that RRV isolates in the U.S. have low genetic diversity and are widely distributed. However, there is limited information on how RRV evolves. In this study, we collected rose samples from garden nurseries, department stores, and natural sources across the state, which were then subjected to RNA isolation. We used reverse transcription polymerase chain reaction (RT-PCR) to screen for RRV-positive samples. Several positive samples were selected for genome sequencing using both Sanger sequencing (with overlapping primers or primer walking) and Illumina high-throughput sequencing. We then combined our annotated RRV genomes with publicly available RRV sequences from the National Center for Biotechnology Information (NCBI) to analyze their phylogenetic relationships. Phylograms were generated for each segment of the RRV genome, and a concatenated phylogenomic analysis was also performed. Our findings suggest that RRV diversity may be increasing or was previously underestimated. In either case, the current understanding of RRV’s diversity should be reconsidered, as our analyses indicate a higher level of diversity within the RRV population. This has significant implications for the rose industry, as new isolates or lineages could further strain efforts to manage RRD.