The Prader–Willi/Angelman syndrome (PWS/AS) locus is regulated by the epigenetic mechanism of parental genomic imprinting. This region holds two eutherian-specific, large tandem repeats of box C/D small nucleolar RNA (Snord) genes called SNORD115 and SNORD116, whose loss of paternal expression is key in the development of the PWS. Snords represent an ancient class of noncoding RNAs that typically direct the 2′-O-methylation of specific nucleotides of ribosomal RNAs. However, Snord115 and Snord116 belong to the large class of orphan Snords whose functions remain unclear. The constraints that generated and maintained their unusual genetic organization for mammalian genomes have been poorly addressed to date. Here, a comparative analysis of the evolutionary history of both tandem repeats reveals that several genetic events affected them concomitantly, including copy gains and losses between species, emergence of gene subfamilies in catarrhines or partial tandem duplication in rats. Several indications suggest that parental genomic imprinting orchestrated this coordination of events, adding a new effect on mammalian genome structure and evolution to its roles in gene dosage, meiotic recombination and replication timing. Finally, our work provides a functional rationale for the existence of closely located tandem repeats of small RNA genes in mammalian genomes.