Epigenetic or non-Mendelian inheritance has been recognized as an integral part of genome regulation in plants and animals. Epimutations (independent of primary DNA sequences) are widespread and can occur naturally and in response to internal (hybridization) and external (environmental) factors. However, the origin, inheritance, and function of epigenetic variation have not been systematically investigated. Here we report genome-wide studies of DNA methylation and epiallele inheritance in three model plants. We found rapid and stochastic epigenetic changes in newly formed Arabidopsis interspecific hybrids and allotetraploids, leading to convergent epigenetic variation in natural allotetraploid A. suecica. These epialleles exhibit cis- and trans-regulation of flowering-time variation and mitotic and meiotic processes that are related to adaptation and speciation. Consistent with the changes in Arabidopsis, epigenetic variations among five allotetraploid cotton species are also found in the extant interspecific hybrid, suggesting maintenance of epialleles over one million years of cotton evolution including domestication and modern breeding. Notably, these epialleles are associated with agronomic and domestication traits, including genes that control photoperiodic flowering, which may facilitate worldwide cultivation of cultivated cotton. The origin of epialleles results from trans-acting small interfering RNAs (siRNAs) via RNA-directed DNA methylation in maize hybrids. The trans-methylation patterns like paramutation are heritable over nine generations of backcrossing and self-pollination. Most epialleles are related to stress responses that may increase potential for adaptation. These principles of epigenetic inheritance will help us explore and utilize a repertoire of epigenomic variation to improve crop yield and resilience through molecular breeding, genome-editing, and epigenetic engineering.