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Whereas recruitment success for many fisheries depends on coincident timing of larvae with abundance peaks of their prey, less can be more in the tropical/subtropical spawning areas of bluefin tunas if lower but steady food resources are offset by reduced larval vulnerability to pelagic predators. To understand larval habitat characteristics for Southern Bluefin Tuna (SBT), we quantified microbial community carbon flows based on growth and grazing rates from depth profiles of dilution incubations and carbon biomass assessments from microscopy and flow cytometry (FCM) during their peak spawning off NW Australia (Indian Ocean) in February 2022. Two Chla-based estimates of phytoplankton production gave differing offsets due to cycling or mixotrophy, exceeding 14C net community production on average (677 ± 98 versus 447 ± 43 mg C m−2 d−1). Productivity was higher than in the Gulf of Mexico spawning area for Atlantic Bluefin Tuna but less than similar studies of oceanic upwelling regions. Microzooplankton grazing averaged 482 ± 63 mg C m−2 d−1 (71 ± 13 % of production). Two measurement variables for Prochlorococcus gave average production and grazing rates of 282 ± 36 and 248 ± 32 mg C m−2 d−1 (86 ± 6 % grazed). Prochlorococcus comprised almost half of production and grazing fluxes in the upper (0–25 m) euphotic zone where SBT larvae reside. Prochlorococcus declined and eukaryotic phytoplankton and heterotrophic bacteria increased in relative importance in the lower euphotic zone. These results describe relatively classic open-ocean oligotrophic conditions as the food web base for nutritional flows to SBT larvae.