Fusarium is a large genus that includes animal and plant pathogenic species as well as saprophytes. Moreover, specimens from this genus are used in biocontrol as well as for industrial applications. We integrated various disciplines on representatives across the genus. Chromosome numbers (CN) were determined using Germ Tube Burst Method (GTBM), and different sequencing platforms were applied to generate high quality assemblies. In several species, remarkable genome plasticity is observed, including variable CNs and the presence of supernumerary chromosomes that differ markedly from the core chromosomes. It appears that several fusion events between core chromosomes happened during speciation. In F. poae, these supernumerary chromosomes (~8 Mb) exhibit marked differences from the core chromosomes: in the core genome only 2.1% consists of transposable elements (TEs) while TEs make up 25% of the supernumerary chromosomes. The TEs in the core genome show clear signs of repeat-induced point mutation (RIP), while no RIP was found in the supernumerary genome. In addition, no paralogous genes are present on the core, but many are found in the supernumerary genome. Exchange of genetic material occurs between the core and supernumerary genomes. Intact TEs from the supernumerary genome integrate into the core chromosomes, where they are subsequently subjected to RIP. In addition, large blocks of sequence (>200 kb) from the supernumerary genome have recently been translocated to the core genome. The reverse also appears to have occurred: genes from the core seem to have undergone duplication followed by translocation of one of the resulting paralogs to the supernumerary genome, where some paralogs may have undergone further duplications. This exchange of genes between the core and supernumerary genomes bestows significant opportunities for adaptation and evolution on the organism. This is reminiscent to the compartmentalization of genetic material in F. graminearum, where non-conserved regions are found at various places on the four core chromosomes.