Assisted reproductive technologies (ART) are commonly used to address human infertility and to boost livestock production. During ART, procedures such as in vitro fertilization, artificial insemination, and intracytoplasmic sperm injection introduce gametes and embryos to unnatural and potentially stressful conditions that can influence offspring health, often via epigenetic effects. In this perspective we summarize these key risks of ART for embryonic and longer-term offspring fitness, emphasizing the need for experimental research on animal models to determine causal links between ART and offspring fitness across multiple generations. We also highlight how ART can bypass a range of naturally and sexually selected mechanisms that occur in the female reproductive tract and/or via female secretions that ultimately determine which sperm fertilize their eggs. We further argue that this curtailment of female-modulated mechanisms of sperm selection may have important consequences for ART-conceived offspring. We encourage the development of ART methods that better mimic natural processes of sperm selection and embrace the fundamental principles of natural and sexual selection. Ultimately, the aim of this perspective is to encourage dialogue between the fields of evolutionary biology and applied areas of animal and human reproduction.