Miniature inverted-repeat transposable elements (MITEs) are a potent source of polymorphisms in plant genomes. A genotyping system, named DcS-ILP, based on polymorphic insertions of Stowaway MITEs (DcStos) localized in introns and identified in the reference genome DH1, has been developed for carrot. Here, we report an extension of the DcS-ILP genotyping system by incorporation of non-reference insertions identified in resequenced genomes representing the eastern gene pool. We genotyped 52 carrot accessions representing the eastern and western carrot gene pools with 92 markers developed previously (western DcS-ILP panel) together with 84 newly developed markers (eastern DcS-ILP panel). Overall, the DcS-ILP markers revealed a highly structured genetic diversity separating the eastern and the western carrot accessions at K = 2 and differentiating Indian breeding lines from the eastern accessions at K = 3. The eastern DcS-ILP panel proved to be more robust with respect to the eastern carrot gene pool, while it provided little information on the western accessions, as many of the DcSto insertions present in the eastern gene pool were absent in the western gene pool. As the western carrot accessions represent improved cultivars, DcSto insertional polymorphisms allowed detection of a selection-driven bottleneck at the improvement stage. Selection in the course of the improvement stage generally operated on standing variation, as the subset of DcSto insertions present in the western carrot likely originated from transposition events preceding the separation of both gene pools. However, occasional frequency shifts in the opposite direction were also revealed, possibly indicating selection for favorable variants associated with DcSto insertions.