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Parasites, of all sorts, can profoundly affect host population dynamics. Parasites commonly cause sex-biased mortality and this can add to their impact. Female-biased mortality in particular can destabilize dynamics and promote population collapse. We previously reported in a correlative study that brown-headed cowbird Molothrus ater brood parasitism of song sparrows Melospiza melodia appears to cause female-biased host nestling mortality. Here, we report results from ‘infestation’ and ‘de-infestation’ experiments designed to test whether brood parasitism causes female-biased mortality, and we document the resulting demographic impact using a simulation model. Experimental cowbird infestation of song sparrow nests halved the proportion of female host nestlings (0.31±0.07 vs 0.59±0.06; infested vs unparasitized nests at day 6) replicating the halving reported in naturally cowbird-parasitized nests (0.28±0.01 vs 0.57±0.05; parasitized vs unparasitized). De-infestation of naturally cowbird-parasitized nests in turn wholly eliminated any effect on the proportion of female host nestlings (0.53±0.13 vs 0.54±0.06; de-infested vs unparasitized) confirming that brood parasitism is the cause. This halving of the proportion of females fledging is likely to be as significant as nest predation in affecting population dynamics, based on the elasticities derived from our demographic model (–0.50 vs –0.59). Experimental infestation reduced the testosterone levels, begging behaviour, and body mass of six day old female host nestlings, whereas males were largely unaffected, suggesting that it is the exacerbation of intra-brood competition that may be primarily responsible for the resulting female-biased mortality. The brown-headed cowbird is invasive in most of North America and has been implicated in regional population declines of many native species. We suggest that female-biased host offspring mortality is likely to be commonplace among the 144 host species the cowbird successfully parasitizes, and we discuss the negative implications for songbird conservation, given the projected demographic impact.