<p>Transposable elements (TEs) are dynamic components of eukaryotic genomes, playing a crucial role in genome evolution and plasticity, particularly in unstable regions such as chromosome ends. In the globally significant fungal pathogen <i>Fusarium oxysporum</i>, we identified and characterized a novel family of non-LTR retrotransposons named FoTeRs (<i>F. oxysporum </i>Telomeric Retrotransposons). These elements are consistently and uniquely localized at chromosome ends, representing a rare example of site-specific TE integration. Phylogenetic analysis confirmed that FoTeRs form a distinct clade with other telomere-targeting retrotransposons, suggesting a shared evolutionary history and a convergent mechanism for telomeric integration. We found that individual FoTeR elements exhibit a duality in their evolutionary status. Putatively functional elements are under strong purifying selection, indicating that their protein-coding regions are highly conserved. This contrasts with the presence of other, non-functional copies that exhibit signs of mutational decay, a process accelerated by Repeat-Induced Point (RIP) mutations —a fungal-specific defense mechanism. The high density of upstream variable number tandem repeats (VNTRs) also contributes to their genomic plasticity. Furthermore, FoTeRs frequently co-localize with host Telomere-Linked Helicases (TLHs), suggesting a potential functional link in telomere maintenance. This study provides crucial insights into the role of TEs in shaping the genome architecture and adaptive potential of this important fungal pathogen.</p>