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Effort spent on raising unrelated offspring can be costly and wasteful, and parents are expected to reduce their level of investment when they have low or uncertain relatedness to the young under their care. Although the relationship between parental certainty and parental investment is theoretically well established, empirical support has been mixed. Here, we report on a series of lab and field experiments that test whether paternal investment is reduced as paternity decreases in the plainfin midshipman fish (Porichthys notatus), a species of toadfish with male-only care. We explored what cues plainfin midshipman males use to assess their paternity. We show that a nest takeover, in which a male displaces another male from a nest, can be a reliable indirect cue of paternity information and leads to a drop in offspring survival. We also show that, when presented in isolation, direct cues of reduced offspring relatedness do not result in a decline in offspring survival in midshipman. Our findings help clarify what systems, species, and theoretical assumptions best reveal the link between parental investment and parentage.