Intracellular partitioning of trace metals is critical to metal tolerance in aquatic organisms and may also influence metal trophic transfer in ecosystems. In this study, we tested the relevance of metal (Cd, Cu, Pb, and Zn) intracellular partitioning in prey as an indicator of metal trophic availability to benthic forage fish, mummichogs (Fundulus heteroclitus), in chronically metal-polluted salt marshes in New York, USA. Two common prey of mummichogs in the study area, Palaemonetes pugio and Nereis acuminata, generally stored increasingly higher proportions of non-essential metals (particularly Pb) in insoluble (less trophically available) cellular components, as the whole body burdens increased. In contrast, intracellular partitioning of essential metals (Cu and Zn) in invertebrate prey varied relatively little among sites. Differential Cd and Pb intracellular partitioning patterns within P. pugio among sites were significantly associated with Cd and Pb whole body burdens in mummichogs, respectively (i.e., prey-driven bioreduction of metals), while bioaccumulation of Cu and Zn in mummichogs was similar among populations. The findings in this study suggest that metal intracellular partitioning within prey may be partially responsible for metal trophic availability to a predator in metal-polluted habitats, while there was also evidence that some predator-dependent processes may offset differential trophic availabilities from prey.