The North American–Greenlandic genus Boechera Á. Löve & D. Löve (Brassicaceae) is distinguished from other phylogenetic lineages recognized within the artificial taxon Arabis L. s.l., in which it has formerly been included, by its base chromosome number x = 7. Based on outgroup comparisons, we consider this chromosome number to be derived from an ancestral genome comprising eight chromosomes. Chromosome counts are now available for about half of the species names listed in the most recent taxonomic treatments of the genus. An analysis of the karyological differentiation with respect to chromosome numbers was performed, and these patterns were correlated with data on pollen viability and population genetic measures in order to deduce modes of reproduction. This approach allowed us to distinguish three main groups: sexual, amphi-apomictic, and apomictic species, respectively. We focused further on the cytology of gametes, especially on that of pollen, and we discuss its role in the formation of new genotypes and cytotypes. Evidence for the following evolutionary phenomena is currently available: (1) allopolyploidization, (2) homoploid hybrid formation, and (3) establishment of viable offspring by means of fusion of highly aneuploid gametes, which resulted from irregular meiotic divisions. In contrast, there is no strict evidence demonstrating the occurrence of autopolyploidization. Boechera experts have just started to integrate evolutionary concepts derived from molecular analyses into taxonomic research, and profound changes, with respect to species definition and circumscription, are to be expected in the near future. The identified modes of reproduction and evolutionary phenomena will contribute to the development of a theoretical and practical basis on which future taxonomic classifications and species concepts can be based.