Bonobos are the only ape species, other than humans, that have demonstrated prosocial behaviors toward groupmates and strangers. However, bonobos have not been tested in the most frequently used test of prosociality in animals. The current study tested the other-regarding preferences of bonobos in two experiments using the prosocial choice task. In the first experiment subjects preferred a food option that would benefit both themselves and another bonobo. This preference was likely the result of a location bias developed in the pretest since they showed the same preference in the non-social control condition within test sessions. A second experiment was designed to help subjects overcome this bias that might interfere with their social choices. Bonobos again did not prefer to choose the prosocial option. However, results suggest constraints of this paradigm in revealing social preferences. In discussing our results we consider why bonobos show robust prosocial preferences in other paradigms but not here. While others have suggested that such contradictory results might suggest interesting motivational or cognitive differences between humans and non-humans, we propose that the current ‘standard’ paradigm has failed validation due to three methodological constraints. Across the dozens of studies completed few have demonstrated that non-human subjects understand the causal properties of the apparatus, non-social biases quickly develop in inadequately counterbalanced pretests that typically explain subjects’ choices in the test, and even human children found this choice task too cognitively demanding to consistently show prosocial preferences. We suggest it is time to consider switching to a variety of more powerful and valid measures.