Many animals time their breeding to the seasons, using the changing day length to forecast those months when environmental conditions favor reproductive success; in Siberian hamsters (Phodopus sungorus), long summer days stimulate whereas short winter days inhibit reproductive physiology and behavior. Non-photic environmental cues are also thought to influence the timing of breeding, but typically their effects on reproduction are minor and more variable under categorically long and short photoperiods. We hypothesized that the influence of non-photic cues might be more prominent during intermediate photoperiods (early-spring and late-summer), when day length is an unreliable predictor of year-to-year fluctuations in food availability. In hamsters housed in an intermediate photoperiod (13.5 h light/day), two non-photic seasonal cues, mild food restriction and same-sex social housing, induced gonadal regression, amplified photoperiod history-dependent reproductive responses to decreasing day lengths, and prevented pubertal development indefinitely. These cues were entirely without effect in hamsters maintained under a long photoperiod (16 h light/day). Thus, intermediate photoperiods reveal a heightened responsiveness of the reproductive axis to non-photic cues. This photoperiod-dependent efficacy of non-photic cues may explain how animals integrate long-term photic and short-term non-photic cues in nature: intermediate day lengths open a seasonal window of increased reproductive responsiveness to non-photic cues at a time when such cues may be of singular relevance, thereby allowing for precise synchronization of the onset and offset of the breeding season to local conditions.