Human menopause is ubiquitous among women and is uninfluenced by modernity. In addition, it remains an evolutionary puzzle: studies have largely failed to account for diminishing selection on reproduction beyond 50 years. Using a 200-year dataset on pre-industrial Finns, we show that an important component is between-generation reproductive conflict among unrelated women. Simultaneous reproduction by successive generations of in-laws was associated with declines in offspring survivorship of up to 66%. An inclusive fitness model revealed that incorporation of the fitness consequences of simultaneous intergenerational reproduction between in-laws, with those of grandmothering and risks of dying in childbirth, were sufficient to generate selection against continued reproduction beyond 51 years. Decomposition of model estimates suggested that the former two were most influential in generating selection against continued reproduction. We propose that menopause evolved, in part, because of age-specific increases in opportunities for intergenerational cooperation and reproductive competition under ecological scarcity.