Southern Bluefin Tuna (SBT, Thunnus maccoyii) spawn only in a small tropical region overlying the Argo Abyssal Plain (Argo Basin) off northwestern Australia. We investigated this region during the peak SBT spawning season (January-March) of 2022 to assess nutrient sources, productivity, pelagic food web structure and their relationships to larval SBT feeding, growth and survival. The study revealed strong system balances among nitrogen inputs, phytoplankton production, micro- and meso-zooplankton grazing, and export in the region, with highly selective feeding on appendicularians resulting in efficient trophic transfer from picophytoplankton-dominated productivity to SBT larvae. Here, we highlight inferences on prey trophic structure and the growth characteristics of larvae that come from more detailed analyses of isotopic composition. Otolith-microstructure ageing was combined with bulk nitrogen and carbon stable-isotope analysis (SIA) to identify individual larvae that were growing fastest (OPT, optimal) and slowest (DEF, deficient). OPT larvae had narrower isotopic feeding niches, indicating resource specialization, and fed on prey closer to the food web base (lower trophic position) than DEF larvae. Among potential zooplankton prey, Compound Specific Isotopic Analyses of Amino Acids (CSIA-AA) identified appendicularians as uniformly having the lowest trophic position (TP = 2.0), corresponding to that of a pure herbivore. Therefore, OPT growing larvae aligned with high dietary specialization on appendicularians. OPT growing larvae also provided isotopic evidence of a significant maternal influence on offspring fitness, characterized by narrow diet of adult females, which enhanced larval survival in a drifter-marked patch that was resampled over the course of 2 weeks. These results underscore the need to consider larval trophodynamics, niche breadth and maternal influences as factors that will modulate growth, predation risk and competitive fitness during early development as climate conditions change.