Mobile transposable elements are among the primary drivers of the evolution of eukaryotic genomes. For fungi, repeat-induced point mutation (RIP) silencing minimizes deleterious effects of transposons by mutating multicopy DNA during meiosis. In this study we identify five transposon species from the mitosporic fungus Colletotrichum cereale and report the signature pattern of RIP acting in a lineage-specific manner on 21 of 35 unique transposon copies, providing the first evidence for sexual recombination for this species. Sequence analysis of genomic populations of the retrotransposon Ccret2 showed repeated rounds of RIP mutation acting on different copies of the element. In the RIPped Ccret2 population, there were multiple inferences of incongruence primarily attributed to RIP-induced homoplasy. This study supports the view that the sequence variability of transposon populations in filamentous fungi reflects the activities of evolutionary processes that fall outside of typical phylogenetic or population genetic reconstructions.