JC polyomavirus (JCV) isolates worldwide are classified into three super-lineages (A, B and C), with A and B further split into several lineages and sub-lineages. The transcriptional control region (TCR) of the JCV genome generally has the archetypal configuration, but rearranged TCRs have occasionally been detected in isolates from immunocompetent individuals. To investigate the phylogenetic significance of these rearrangements, we analyzed 298 TCR sequences all derived from complete JCV genomes directly cloned from the urine of non-immunocompromised individuals. While sporadic rearrangements were found in many lineages and sub-lineages, common rearrangements were identified in all, or essentially all, isolates belonging to particular lineages or sub-lineages. Interestingly, several common rearrangements were also detected as sporadic rearrangements in other lineages or sub-lineages. This observation suggests that during the course of JCV evolution, JCV strains with sporadic rearrangements became predominant over archetypal TCRs in some JCV lineages or sub-lineages.