Centromeres are chromosomal structures required for faithful genome inheritance during cell division. Centromeres are defined epigenetically by the presence of the centromere-specific histone H3 variant, CENP-A. While centromeres form in repeat-rich regions of the genome, the roles of DNA sequences in centromere function are unclear. We recently revealed that all centromeres in D. melanogaster correspond to islands of complex DNA enriched in retroelements and flanked by tandem repeats. Each centromere is unique—the only sequence they have in common is the G2/Jockey-3 retroelement. It is unclear if any of these sequences are important for centromere function. Here we study the evolution of centromere composition to gain insights into the role of DNA sequence in centromere biology. We combined (epi)genomic and cytological approaches to characterize centromere organization in three sister species: D. simulans, D. sechellia, and D. mauritiana. We discovered dramatic centromere reorganization involving recurrent shifts between retroelements and satellite DNAs over short evolutionary timescales (<240 Kya). None of the D. melanogaster centromere islands are conserved in the simulans clade. Instead, in the simulans clade centromeres are mainly composed of two complex satellites: 500bp and 365bp. Those two complex satellites are specific to the simulans clade, suggesting that they invaded and replaced centromeres after the split with D. melanogaster. In addition, we observed a second replacement event specific to D. sechellia, where the dot and X chromosome centromeres now sit on telomere-specific retroelements, revealing for the first time true telocentric chromosomes. Finally, G2/Jockey-3 is enriched in D. simulans centromeres, but much less so in D. sechellia and D. mauritiana. Identifying the functional centromeric DNA shed new light into their roles in chromosome function and evolution. Our results highlight the very rapid turnover of centromeric sequences among the melanogaster clade and are consistent with recurrent genetic conflict.