SignificanceRetrotransposons are mobile genetic elements that occupy a large fraction of eukaryotic genomes, but are generally regarded as genomic parasites that do not contribute to host biology. This study reveals that the Drosophila retrotransposon R2 has a function essential to maintain its hosts genome. R2 specifically mobilizes within the large number of tandem ribosomal DNA (rDNA) repeats needed for proper ribosomal function. rDNA repeats are frequently lost from the genome, and restoration of these lost copies within the germline is required to maintain rDNA over successive generations. We find that R2 activity stimulates the expansion of rDNA copies needed to maintain rDNA throughout a population, indicating that R2 mutually benefits the survival of its host genome and its own propagation.