The classical version of the differential allocation hypothesis states that, when females reproduce over their lifetime with partners that differ in their genetic quality, they should invest more in reproduction with high-quality males. However, in species with lifetime monogamy, such as the zebra finch, partner quality will typically remain the same. In this case, the compensatory investment (CI) hypothesis predicts higher investment for low-quality males, because low genetic quality offspring are more dependent on maternal resources. Here, we show that female zebra finches invested more resources, both in terms of egg volume and yolk carotenoid content, when paired to a low genetic quality male, as judged from his previous ability to obtain extra-pair paternity in aviary colonies. We also found that females deposited slightly larger amounts of testosterone into eggs when paired to a low parental quality male, as judging from his previous success in rearing offspring. This is, to our knowledge, the first experimental support for the CI hypothesis in a species with lifetime monogamy. We stress that in more promiscuous species, the benefits of classical differential allocation may partly be neutralized by the supposed benefits of CI.