Thrips-transmitted tomato spotted wilt orthotospovirus (TSWV) is a major constraint to peanut production in the southeastern United States. Peanut cultivars with resistance to TSWV have been widely used for over twenty years. Intensive usage of resistant cultivars has raised concerns about possible selection pressure against TSWV and a likelihood of resistance breakdown. Population genetics of TSWV isolates collected from cultivars with varying levels of TSWV resistance was investigated using five TSWV genes. Phylogenetic trees of genes did not indicate host resistance-based clustering of TSWV isolates. Genetic variation in TSWV isolates and neutrality tests suggested recent population expansion. Mutation and purifying selection seem to be the major forces driving TSWV evolution. Positive selection was found in N and RdRp genes but was not influenced by TSWV resistance. Population differentiation occurred between isolates collected from 1998 and 2010 and from 2016 to 2019 but not between isolates from susceptible and resistant cultivars. Evaluated TSWV-resistant cultivars differed, albeit not substantially, in their susceptibility to thrips. Thrips oviposition was reduced, and development was delayed in some cultivars. Overall, no evidence was found to support exertion of selection pressure on TSWV by host resistance in peanut cultivars, and some cultivars differentially affected thrips fitness than others.