Avian leukosis subgroup J (ALV-J) causes a variety of tumors and mortality in meat-type chickens. Since its discovery in the late 1980s, ALV-J has spread to breeding stock produced by most primary breeding companies of North America, the European Union, and Asia. ALV-J seems to have been eradicated from elite breeding stock produced by most primary breeders, albeit ALV-J still circulates in some commercial poultry. This study was undertaken to examine the molecular epidemiology and evolution of ALV-J detected in breeding stock and broiler chickens representing eight primary breeding companies over a period of approximately 20 yr (1988–2007). The redundant transmembrane region of the envelope gene has been deleted in some isolates, suggesting that this region is dispensable for viral fitness. Within the 3′ untranslated region (3′ UTR), the direct repeat 1 was present in 100% of the ALV-J isolates studied. In contrast, the E element has undergone substantial deletions in >50% of the ALV-J proviruses studied. Overall, the unique region 3 was the least conserved within the 3′ long terminal repeat (LTR), albeit the transcriptional regulatory elements typical of avian retroviruses (CAAT, CArG, PRE, TATA, and Y boxes) were highly conserved. The direct repeat region of the LTR was identical in all of the proviruses, and the 3′ unique region 5 was relatively well conserved. Thus, the 3′ UTR of ALV-J has evolved rapidly, reflecting significant instability of this region. Some of the mutations in the 3′ UTR have resulted in the emergence of moderately distinct genetic lineages representing each primary breeding company from which ALV-J was isolated.