Reverse transcriptases have shaped genomes in many ways. A remarkable example of this shaping is found on telomeres of the genus Drosophila, where retrotransposons have a vital role in chromosome structure. Drosophila lacks telomerase; instead, three telomere-specific retrotransposons maintain chromosome ends. Repeated transpositions to chromosome ends produce long head to tail arrays of these elements. In both form and function, these arrays are analogous to the arrays of repeats added by telomerase to chromosomes in other organisms. Distantly related Drosophila exhibit this variant mechanism of telomere maintenance, which was established before the separation of extant Drosophila species. Nevertheless, the telomere-specific elements still have the hallmarks that characterize non-long terminal repeat (non-LTR) retrotransposons; they have also acquired characteristics associated with their roles at telomeres. These telomeric retrotransposons have shaped the Drosophila genome, but they have also been shaped by the genome. Here, we discuss ways in which these three telomere-specific retrotransposons have been modified for their roles in Drosophila chromosomes.