The whole-body transcriptome of trout alevins was characterised to investigate the effects of long-term feeding of rainbow trout broodstock females a diet free of fishmeal and fish oil on the metabolic capacities of progeny. Effects were studied before first feeding and after 3 weeks of feeding diets containing different proportions of marine and plant ingredients. Feeding alevins plant-based diets resulted in lower fish body weight, irrespective of maternal nutritional history. No differences in whole-body lipids were found between treatments, and the tissue fatty acid profile strongly reflected that of the respective broodstock or first-feeding diets. We showed that the maternal diet history did not significantly affect expressions of any genes before the first feeding. Interestingly, we found an effect of maternal nutritional history on gene expression in alevins after 3 weeks of feeding. The major differences in the transcriptome of alevins from plant-based diet-fed females compared with those from commercial-fed females were as follows: (i) down-regulation of genes involved in muscle growth/contraction and (ii) up-regulation of genes involved in carbohydrate and energy metabolism related to the delay in growth/development observed with plant-based diets. Our findings also showed an effect of the first-feeding diets, irrespective of maternal nutritional history. Specifically, the introduction of plant ingredients resulted in the up-regulation of genes involved in amino acid/protein and cholesterol metabolism and in differences in the expressions of genes related to carbohydrate metabolism. Information gained through this study opens up avenues for further reduction of marine ingredients in trout diets, including the whole rearing cycle.