Allopolyploidy, i.e., coupling of interspecific hybridization and whole genome duplication (WGD), has been widely documented as a prominent evolutionary force driving speciation, evolution and diversification of angiosperms. One source of genetic variation associated with allopolyploidy is genome repatterning immediately following allopolyploidy due to incompatible genetic interactions between the suddenly merged subgenomes derived from different species, a revolutionary insight first envisioned by Barbara McClintock, who coined the term “genome shock”. Nonetheless, the scope and extent of such genome repatterning, especially in aspect of karyotype diversification and its relevance to phenotypic innovation, remains to be fully understood. Here, we karyotyped a total of 1322 individuals at the 8th selfed generation (S8) descended from a single S2 euploid founder plant of a synthetic allotetraploid wheat (genome SSDD) parented by two Aegilops species, Ae. bicornis (SS, maternal) and Ae. tauschii (DD, paternal). We identified extensive chromosomal variations in both number (numerical chromosomal variation, abbreviated NCV) and structure (structural chromosomal variation, abbreviated SCV) in this set of plants. The combinatory and transgenerationally accumulative features of NCVs and SCVs generated massive organismal karyotypic heterogeneity at the population level. Substantial differences were found in both NCVs and SCVs across the seven sets of homoeologous chromosomes. Further analyses revealed that NCVs and SCVs were intrinsically linked and both were generated by meiotic chromosomal irregularity (such as multivalent and heteromorphic bivalent formation) and constrained by compensation capacity between homoeologous chromosomes. Moreover, both properties varied markedly across the homoeologous chromosome pairs, and were correlated with both overall sequence similarity and proportions of concatenated length (nt) of syntenic genes. A wide range of phenotypic diversity was manifested by these karyotypically variable plants. Together, our results demonstrate that virtually unlimited karyotype variability can be rapidly generated by a single allopolyploidization event, which may facilitate evolution and promote generation of useful germplasm resource for crop improvement.