Pivotal-differential genome relationships in the wheat (Triticum and Aegilops genera) group refer to the pattern whereby one genome in an allopolyploid is relatively conserved (pivotal) between diploid and allopolyploid wheat group species, whereas the other genome(s) is altered (differential) relative to other diploid and allopolyploid species containing this genome. This pattern was first identified based on comparative morphology (flowering spikes), whereby species could be grouped into A, D and U genome clusters. However, substantial cytogenetic evidence also supports this genome relationship, and with recent genomic advancements in wheat we suggest that it is time to interrogate this relationship further, and to extend these concepts to other plant taxa where it may be relevant. In particular, we propose that pivotal differential genome patterning within taxa may have three possible explanations that should be tested. Firstly, variation between species sharing a differential genome may be directly inherited from variation (e.g. different progenitor cytotypes or subspecies) present within the ancestral diploid species. Secondly, variation between species may be induced as a result of the allopolyploid formation event, perhaps as a result of dominance relationships between subgenomes. Thirdly, hybridization between two allopolyploid species that share a (pivotal) genome in common but differ in their second genome may give rise to a new, rearranged (differential) genome after hybridization and genome stabilization (e.g. AABB x AACC -> AADD). Interrogation of future pan-genome data coupled with synthetic recreation of historical hybridization events is predicted to reveal the mechanisms underlying pivotal-differential genome patterns.