Illumina-MiSeq next-generation sequencing of ITS 5.8S rRNA gene demonstrated the transgenerational transmission of fungal seed-endophytes (mycobiome) across three consecutive wheat host generations under standard-control and drought conditions in the greenhouse. Drought-stressed plants experienced a positive shift in the seed mycobiome's composition, moderated by the external acquisition of endophytic Penicillium (E+) at the seed level. Untreated (E-) and unstressed plants harbor a maximal fungal diversity of non-equilibrium ecological communities. While fungal composition in drought-stressed E- plants experienced important fluctuation, E+ plants maintained fungal ecological communities in phase equilibrium across generations. E+ plants hosted a relatively higher abundance of Ascomycota in the 2nd and 3rd seed generations of wheat, whereas higher abundance of Basidiomycota was detected in 1st generation seeds. The dynamic response of ecological communities to environmental stress is conducive to E+ plants' active recruitment of endosymbiotic consortia in seeds, benefiting host stress resilience and phenotype. In contrast, E- plants showed an erratic distribution of detected OTUs with an increased occurrence of phytopathogens and diminished plant performance under stress. The present study gives insight into the understanding of the seed-mycobiome composition and dynamics with the potential to improve plant host traits in an adverse environment.