Centromere repositioning is a well-documented phenomenon in mammals and plants. It involves the formation of a new centromere on the same chromosome without disrupting genome colinearity and contributes to genome evolution and reproductive isolation. However, the origin, structure and evolution of evolutionary new centromeres (ENCs) remain largely unexplored. To address this gap, we performed de-novo genome assemblies of six Arabideae species using PacBio HiFi and ONT nanopore reads. For four species (Draba nemorosa, D. podolica, Arabis auriculata, and the early diverging Pseudoturritis turrita) we achieved telomere-to-telomere chromosome-level assemblies, along with scaffold-level assemblies for A. cypria and Pachyneurum grandiflorum. Both Draba species share a common chromosome structure and relative centromere positions, Pa. grandiflorum is structurally similar to Arabis alpina and A. montbretiana, while the genome of A. Auriculate originated by descending dysploidy (from n = 8 to n = 7). In Ps. turrita paleocentromeres consist of four tandem repeats (monomer size 149, 176, 186 and 63 bp) and LTR retroelements (Ale, CRM, Retand). Compared to the paleocentromeres, the ENCs were repositioned by 4 Mb (median) in D. nemorosa, by 17 Mb in D. podolica, by 11 Mb in Pa. grandiflorum and by 6 Mb in A. auriculata. We provide a detailed sequence and epigenetic characterization of homeologous paleocentromeric sites and ENCs and infer the mechanism of centromere repositioning in the Arabideae.