Integrated breeding strategies are used to increase both the yield potential and stability of crops. Most of these approaches have a direct genetic basis. The utility of epigenetics in breeding to improve complex traits such as yield and stress tolerance is not clear. A better understanding of the status of the epigenome and its contribution to the agronomic performance would help in developing strategies to incorporate the epigenetic component of complex traits in breeding, Starting from isogenic canola lines, epilines were generated by selecting recursively during three generations for lines with a higher energy use efficiency and drought tolerance. These epilines were more energy use efficient, drought tolerant, high nitrogen use efficient, and higher yielding under suboptimal conditions. Moreover, these characteristics were transgenerational inheritable. Transcriptome comparison with a line selected for energy use efficiency only revealed common differentially expressed genes related to the onset of signaling events regulating stress tolerance. Genes related to salt, osmotic, abscisic acid and drought were specifically differentially expressed in the drought tolerant epilines. The status of the epigenome, scored as differential trimethylation of lysine 4 of histone 3, supports the energy use efficient and drought tolerant phenotype by facilitating transcription of the genes that are found to be differentially expressed.