Intrapopulation variation in habitat use is commonly seen among mobile animals, yet the mechanisms maintaining it have rarely been researched among untrackable species. To investigate how alternative life histories are maintained in a population of the loggerhead sea turtle (Caretta caretta), cumulative reproductive output was evaluated and compared between small planktivores inhabiting oceanic areas (with water depths >200 m) and large benthivores inhabiting neritic areas (depths <200 m) that sympatrically nested at Yakushima Island, Japan, from 1986 to 2011. In total, 362 nesting females sampled in three different years were classified into the two foraging groups based on stable isotope ratios in egg yolks. There were significant differences between the two foraging groups in most recorded life history parameters (clutch size, clutch frequency, breeding frequency, and remigration intervals), with the exception of emergence success. We did not find evidence of life history trade-offs, nor age-related changes in fecundity. Over the 26-year study period, we calculated a 2.4-fold greater reproductive output for neritic foragers than for oceanic ones, accounting for breeding and clutch frequency. Temporal consistencies in stable isotope ratios and remigration intervals within females suggested that female Japanese loggerheads show fidelity to respective foraging habitats throughout the adult stage. The large difference in productivity between the two groups was unlikely to be offset by the difference in survival during the period from aboveground emergence to first reproduction, suggesting that oceanic foragers have a lower level of fitness than neritic ones. Together with an absence of genetic structure between foraging groups, we infer that alternative life histories in a loggerhead turtle population are maintained by a conditional strategy.