We show that genome evolution in the crucifer tribe Biscutelleae (c. 60 species, 5 genera) was dominated by pervasive hybridizations and subsequent genome duplications. By using complementary cytogenomics and phylogenomics approaches, we demonstrate that the origin of a monophyletic plant clade can be more complex than a parsimonious assumption of a single whole-genome duplication (WGD) spurring post-polyploid cladogenesis. Recurrent hybridization among the same and/or closely related parental genomes may phylogenetically interlink diploid and polyploid genomes despite the incidence of multiple independent WGDs. Our results elucidate challenges in resolving the contentious relationships within and between land plant lineages with pervasive hybridization and WGDs. The fascinating evolutionary jigsaw puzzle was published by Molecular Biology and Evolution.