Hybridization and genome doubling (allopolyploidy) have led to evolutionary novelties as well as to the origin of new clades and species. Despite the importance of allopolyploidization, the dynamics of post-polyploid diploidization (PPD) at the genome level has been only sparsely studied. The Microlepidieae (MICR) is a crucifer tribe of 17 genera and c. 56 species endemic to Australia and New Zealand. Our phylogenetic and cytogenomic analyses revealed that MICR originated via an inter-tribal hybridization between ancestors of Crucihimalayeae (n = 8; maternal genome) and Smelowskieae (n = 7; paternal genome), both native to the Northern Hemisphere. The reconstructed ancestral allopolyploid genome (n = 15) originated probably in north-eastern Asia or western North America during the Late Miocene (c. 10.6 - 7 million years ago) and reached the Australian mainland via long-distance dispersal. In Australia, the allotetraploid genome diverged into at least three main subclades exhibiting different levels of PPD and diversity: 1.25-fold descending dysploidy (DD) of n = 15 → n = 12 (autopolyploidy → 24) in perennial Arabidella (3 species), 1.5-fold DD of n = 15 → n = 10 in the perennial Pachycladon (11 spp.), and 2.1 to 3.75-fold DD of n = 15 → n = 7 - 4 in the largely annual crown group genera (42 spp. in 15 genera). These results are among the first to demonstrate multi-speed genome evolution in taxa descending from a common allopolyploid ancestor. It is suggested that clade-specific PPD can operate at different rates and efficacies, and can be tentatively linked to life histories and the extent of taxonomic diversity.