Nutritional intervention with vegetable oils (VO) supplemented to fish broodstock diets enhances progeny ability to utilize low fish meal (FM) and fish oil (FO) diets. However, the intervention with vegetable meals (VM) in broodstock diets has been scarcely tested in marine fish. This study aims to determine the effect of FM replacement by VM alone or in combination with FO replacement by VO as a programming tool. Different broodstocks of gilthead sea bream were fed one of three diets: one contained 35% FM and 10% FO, another contained VM in replacement of FM (FM: 15%) or a third one had both VM and VO in replacement of FM and FO (15% FM and 2.7% FO). At the weight of 3 g, their offspring were challenged with a low FM (5%) and FO (3%) diet for 45 days. FM replacement by VM in broodstock diets did not affect fish reproductive performance but in offspring juveniles reduced growth and feed efficiency and in liver, altered fatty acids profiles and downregulated fatty acyl desaturase 2 (fads2) expression. Combined supplementation of VM and VO in broodstock diets led to a poor reproductive performance, reducing female fecundity and the egg content in eicosapentaenoic acid (EPA) and docosahexanoic acid (DHA). At molecular level, the expression of fads2 and target of rapamycine (tor) genes in the eggs were upregulated. Similarly, in liver of juvenile progenies fads2 and elongase of very long chain fatty acids 6 (elovl6) expression were up-regulated, whereas fads2 expression was correlated to sterol regulatory element-binding protein transcription factor 1 (srebp1). However, methylation rates of CpG rich regions in fads2 promoter were not significantly different among juvenile groups. Thus, the replacement of FM by VM, alone or in combination with FO in diets for gilthead sea bream broodstock negatively affected growth performance of juvenile offspring, whereas the replacement of FO by VO enhanced the fatty acid desaturase and elongase activities in the offspring, especially when juveniles were fed a diet with a high replacement of FM and FO by VM and VO.