A major cause of lameness in turkeys is reoviral arthritis, driven by turkey reovirus (TRV) infection. In the U.S., TRV was first isolated in the 1980s but re-emerged as a significant pathogen causing arthritis in 2011. Since then, TRV outbreaks have spread nationwide across turkey-producing regions and have occasionally resulted in hepatitis-associated pathotypes. The absence of a consistently effective commercial vaccine continues to hinder disease control efforts. To better understand TRV’s evolutionary trajectory and transmission dynamics, we analyzed 211 complete TRV genome sequences collected across the U.S. from 2007 to 2021. Bayesian time-scaled phylogenetic and phylogeographic analyses were conducted for all ten genome segments to estimate gene flow among geographic regions, client groups, and pathotypes. The results reconstructed a coherent, decades-long history of TRV evolution, which revealed segment-specific differences in the evolutionary rates—particularly in S1c (σC protein coding region of S1) and M2—suggesting reassortment with other avian reoviruses during the 2011 emergence. Nationwide spread patterns indicated dominant transmission routes from the Eastern U.S. to Minnesota and from breeder to smallholder flocks, likely driven by inter-regional animal or feed movement via the multi-stage turkey production cycle. Pathotype transitions were more frequently observed from arthritis-associated strains to those causing hepatitis or cardiac lesions. These findings provide crucial insights to support national TRV control strategies and long-term monitoring by industry stakeholders.