Centromeres are indispensable for accurate chromosome segregation, but are subject to rapid sequence turnover while maintaining conserved functions--a paradox in genome evolution. To unravel this paradox, we integrated over 400 fully resolved centromeres from 17 diploid angiosperms spanning 180 million years of divergence, along with 1,000+ pan-genomic assemblies, resequencing datasets, and congeneric whole-genome sequences. We showed that angiosperm centromere organization is determined by lineage-specific combinations of satellite repeats and transposable elements (TEs), which, in turn, shape distinct epigenetic landscapes and evolutionary trajectories within centromeres. In particular, TE insertion patterns were found to be key drivers of structural diversification and positional shift of centromeres in angiosperms. Intriguingly, population-level analyses revealed considerable plasticity in centromere sequences across species, with satellite repeats serving as focal points of evolutionary change and exhibiting species-specific heterogeneity patterns. Temporal reconstructions across congeneric species revealed the emergence and subsequent differentiation of centromeric repeats, outlining a dynamic continuum from gradual sequence diversification to complete turnover during speciation, often accompanied by karyotype reorganization. By integrating intra- and inter-species comparisons, we propose a unifying framework in which centromere innovation is governed by a delicate interplay between genome evolution, chromosomal shuffling, and selection constraints, resulting in phylogenomic signatures of centromere-driven speciation.