Hypocrea jecorina is the sexual form of industrial workhorse fungus Trichoderma reesei that secretes cellulases and hemicellulases to degrade lignocellulosic biomass into simple sugars, such as glucose and xylose. The Hypocrea jecorina CBS999.97 wild isolate undergoes sexual development to produce fruiting bodies containing asci with 16 linearly arranged ascospores (the sexual spores specific to ascomycetes). By genetic and genomic analyses, we show that the 16 ascospores are generated via meiosis followed by two rounds of postmeiotic mitosis. We also found that the genome of the CBS999.97(1-2) haploid is similar to that of ancestral T. reesei strain, whereas the CBS999.97(1-1) haploid genome contains a reciprocal arrangement between two scaffolds of the CBS999.97(1-2) genome. Sexual crossing of these two haploids frequently (>90%) generates asci with viable or inviable ascospores with segmental aneuploidy (SAN). The viable SAN progeny produced white conidia and higher levels of hemicellulases due to segmental deletion and duplication, respectively. Moreover, they readily lose the duplicated segment approximately two weeks after germination. With better lignocellulosic biomass degradation capability, these SAN progeny may provide adaptive advantages to the natural environment, especially in the early phase of colonization.