Vesicular stomatitis (VS) is an arthropod-borne viral disease that negatively impacts domestic livestock and wildlife hosts, and economically impacts both private animal owners and the commercial livestock industry. Previous phylogenetic studies, based on partial P gene sequences, suggested that outbreak cycles of the virus (VSV) exhibit a two-phase dynamic (i.e., incursion and expansion). A single viral lineage from endemic areas of Mexico introduced into the southern United States during an incursion year (2004), can overwinter, and then expand throughout the western United States during the subsequent spring and summer seasons (2005). Our objective was to build on this past research using full-length viral genomic sequences from Mexico and the United States from the same outbreak, and a large suite of geospatial data to identify the environmental factors that influence VSV evolution in the United States and potentially drive the incursion-expansion dynamics. Our phylogeographic analysis confirmed that a single VS New Jersey virus (VSNJV) lineage initiated the 2004 incursion year outbreak was subject to decreasing genetic divergence during the 2004-2006 outbreak cycle, and likely overwintered between the 2004-2006 outbreak seasons. However, rather than a simple geographic relationship, viral genetic sublineages or patristic groups identified as part of our study, were found to be associated with seasonally varying evaporative demand, soil moisture, and precipitation. Our results suggest a functional role for these environmental factors in shaping the evolution and ecology of VSNJV. We speculate a nexus to insect-vector switching and possible adaptation to local environmental conditions to help explain the observed incursion-expansion dynamic in the United States in the 2004-2006 outbreak. Our approach of linking the phylogeography of a virus with the ecology of insect vectors can be applied to other vector-borne diseases.