Self-other distinction is a crucial aspect of social cognition, as it allows us to differentiate our own mental and emotional states from those of others. Research suggests that this ability might be impaired in individuals with autism spectrum disorder (ASD), but convincing evidence of self-other distinction deficits in the emotional domain is lacking. Here we aimed at evaluating emotional self-other distinction abilities in adults with and without ASD, in two behavioral pilot studies and one fMRI study. By using a newly developed virtual ball-tossing game that induced simultaneous positive and negative emotional states in each participant and another person, we were able to measure emotional egocentric and altercentric biases (namely the tendency to ascribe self-/other-related emotions to others/ourselves, respectively). Despite no behavioral differences, individuals with ASD showed decreased activation 1) in the right temporoparietal junction (rTPJ) during active overcoming of the emotional egocentric bias vs. passive game viewing, and 2) in the right supramarginal gyrus (rSMG) during ego-vs. altercentric biases, compared to neurotypical participants. These results suggest a different recruitment of these two regions in ASD when dealing with conflicting emotional states of oneself and another person. Furthermore, they highlight the importance of considering different control conditions when interpreting the involvement of rTPJ and rSMG during self-other distinction processes.