Human-wildlife interactions (HI) are becoming more prevalent with increasing human population. These interactions could have important eco-evolutionary consequences that become apparent only after observing populations for multiple generations. Here, we analyzed 28 years (1993–2020) of data from the world’s longest-running study of a wild dolphin population to assess the fitness consequences of HI on common bottlenose dolphins (Tursiops truncatus) in Sarasota Bay, Florida. We investigated how human-related foraging activities such as depredation, begging, and patrolling mediate reproductive output and reproductive success of conditioned (HI) and unconditioned (non-HI) females. The analysis of 84 females and their 286 calves born during 1993–2020 found a confluence of effects on individual fitness. Reproductive output of females engaging in moderate levels of human-related foraging was 94% greater than that of non-HI females. However, high frequencies of human-related foraging had a negative effect on female reproductive success by increasing the risk of calf death up to nine times when compared to non-HI females, resulting in 31% less calf survival. These findings provide evidence that human-wildlife interactions have considerable potential to catalyze population-level changes by altering individual fitness, and demonstrate the value of comprehensive, long-term data to better understand the ecological and evolutionary implications of human-wildlife conflict.