Despite their essential function in chromosome segregation, centromeres reside in rapidly evolving, repeat-rich genomic regions. Across organisms, centromeres are rich in selfish genetic elements like transposable elements and satellite DNAs that can bias their transmission through meiosis, but still need to contribute to centromere function. To gain insight into the balance between conflict and cooperation at centromeric DNA, we take advantage of the close evolutionary relationships within the Drosophila simulans clade - D. simulans, D. sechellia, and D. mauritiana - and their relative, D. melanogaster. We discovered dramatic centromere reorganization involving recurrent shifts between retroelements and satellite DNAs over short evolutionary timescales. We also reveal the recent origin (<240 Kya) of truly telocentric chromosomes in D. sechellia, where X and dot centromeres now sit on telomere-specific retroelements. This rapid centromere turnover is consistent with genetic conflicts in the female germline and has implications for centromeric DNA function and karyotype evolution.