The Islands of Ulleungdo and Dokdo, with about 40 endemic species, represent excellent cases for the study of plant evolution. Arabis takesimana, a species endemic to Ulleungdo Island, provides an exceptional case in which both derivative and its progenitor species occur together on the island. While A. takesimana is distributed in deciduous forests of the island, its progenitor, A. stelleri, grows on rocky crevices and in sandy soil at the seashore. We investigated the phylogenetic relationships of the species and its closely related species, A. stelleri, A. erecta and A. hirsuta, based on genome-wide SNP data and chloroplast DNA sequences. A total of 83,852 SNP loci were obtained from a genotyping-by-sequencing (GBS) analysis for 96 individuals from 20 populations. Sixteen haplotypes were produced based on chloroplast regions of atpB-rbcL, matK, ndhC-trnV, and ycf1 for 196 individuals from 40 populations. Results of phylogenetic and network analyses indicate that the Arabis individuals may be grouped by distinct phylogeographical regions, not by species. These include (1) the northern region of the East Sea Rim (ESR); (2) the southern region of the ESR; (3) southern South Korea and Kyushu Island of Japan; and (4) the interior region of the Korean Peninsula. Our data suggest that A. takesimana is differentiated as a species endemic to Ulleungdo, followed by genetic introgression from A. stelleri, which immigrated to the island secondarily. This study shows that combining genome-wide SNP and chloroplast haplotype data provides powerful tools to resolve phylogeographic patterns in recently evolved, closely related species.