The development of antipredator traits is dependent on the frequency and intensity of predator exposure over evolutionary and ecological time. We hypothesized that prey species would respond with increasing accuracy when exposed to predators across generational, ontogenetic, and immediate time scales. We assessed larval Pacific chorus frog (PSRE; Pseudacris regilla) individuals that varied in population sympatry, embryonic conditioning, and immediate exposure to stocked populations of rainbow trout (Oncorhynchus mykiss). Using PSRE populations from sites with and without resident rainbow trout, we conditioned embryos to trout odor, PSRE alarm cues, trout odor in combination with alarm cues, or control water. After being hatched and reared in control water, individuals were exposed to the four predator cue treatments using a fully factorial design. Tadpoles from populations with resident rainbow trout did not behave or develop differently than tadpoles originating from fishless sites. However, we found evidence that PSRE reduced predation risk with a combination of carry‐over effect (i.e., transfer of information across life history stages) and within‐life stage phenotypically plastic mechanisms. We found both developmental and behavioral carry‐over effects: tadpoles conditioned with trout odor as embryos grew more slowly and took refuge more often than control animals. Within‐life‐stage behavioral plasticity was observed in tadpoles from all treatment groups, responding to predator cues with increased refuge use. Potentially additive effects of predator exposure on prey response should be considered when predicting the ability of prey to recognize novel threats.