The common octopus, Octopus vulgaris, is a promising mollusc species for marine aquaculture diversification due to its high growth rates and commercial value. Yet, the elevated mortalities mainly related to lipid-linked nutritional deficiencies during the planktonic stage (paralarvae), hinder the development of efficient protocols for a complete rearing cycle. Although the effect of dietary lipids, especially fatty acids (FA), has been the subject of intense research, the available information is essentially restricted to their impact on the composition of the whole parlarval organism. In contrast, little is known about the effects of dietary signature and the specific requirements of each anatomical structure through the paralarvae development. In addition, knowledge about the endogenous capacity in each paralarvae body structure for adaptation to different dietary scenarios is necessary. In the present work, a series of experiments were carried out based on newly hatched paralarvae (PH) and paralarvae fed (30 days post-hatch (DPH)) either with marine crustacean zoeae (PZ) or with Artemia metanauplii (PA). At the end of the trials, the paralarvae were dissected into functional (mantle, head, and arms) and digestive (digestive gland (DG)) body compartment and the FA profile, as well as the expression patterns of genes involved in the long chain polyunsaturated FA (LC-PUFA) (stearoyl-CoA desaturase (scd), ωx2 desaturase (ωx2), ωx1 desaturase (ωx1), fatty acyl desaturase (fad), elovl2/5, elovl4), and glycerophospholipid biosynthetic pathways (agpta, lpin, chpt, and dgat) were analysed. Results showed a positive effect of the PZ diet on growth and development of paralarvae as compared to PA, and distinct FA composition for the 3 experimental groups. The digestive gland was associated to 18C FA (18:3n-3, 18:4n3, 18:1n9, and 18:2n6), while n-6 and n-3 LC-PUFA (20:4n6, 20:5n3, 22:5n3, and 22:6n3) were found in a higher proportion in functional body compartments. The expression of LC-PUFA biosynthesis-linked genes increased significantly during development, with the functional body compartments of the PA treatment being up-regulated as compared to PZ, pointing at a putative compensatory mechanism. In addition, a higher amount of transcripts linked to the triggering of the phosphatidylcholine synthesis (chpt) was found in the digestive gland of PA and PZ and arms of PZ; whereas genes related with triacylglycerol (TAG) synthesis (lpin and dgat) were enhanced in the digestive gland of PA and PH. Dietary treatments affected the FA profile and the gene expression patterns in both digestive (more similar FA profile and glycerophospholipid biosynthesis) and functional (different FA profile and LC-PUFA biosynthesis) compartments of the paralarvae. Furthermore, LC-PUFA biosynthesis-related genes in the head and glycerophospholipid target genes in DG could be used as biomarkers of nutritional deficiencies in paralarvae.