Background Positive symptoms of schizophrenia and its extended phenotype—schizotypy—are characterized by the inclusion of novel, erroneous mental contents. These positive symptoms occur across those with a variety of diagnoses, including schizophrenia, personality disorders, and depression and bipolar with psychotic features. One promising transdiagnostic framework for explaining positive symptoms involves “apophenia,” or the tendency to perceive meaningful patterns where none, in fact, exist. Though hallucinations and delusions represent extreme instances of apophenia, it also occurs throughout the population and can include any instance of a false positive cognition, including such benign occurrences as seeing animals in the clouds or hearing your name in noise. Importantly, apophenia may be the result of heightened pattern seeking in both perception and belief, a tendency that is, along with apophenia and positive schizotypy, positively associated with the personality trait openness to experience. We propose that pattern detection and associated personality and psychopathological traits are, in turn, underlaid by neural networks associated with experiential simulation and cognitive control, specifically, the default and frontoparietal networks. Both of these networks have been implicated in research on psychosis, schizotypy, and openness. Methods Despite consistently demonstrated associations among openness, positive schizotypy, and apophenia, few studies have investigated relations between schizotypy and behavioral manifestations of apophenia, let alone the role of normative personality variation or underlying neural substrates. To investigate these associations, we conducted a series of studies (total N > 3000) using self-report questionnaires, behavioral indicators of pattern detection sensitivity, and functional magnetic resonance imaging (fMRI). Results Across samples, robust positive associations were found among openness, positive schizotypy, and psychotic-like experiences. In turn, all three of these traits were positively associated with general tendencies toward false positive errors, including perceiving social intentions or emotions when none were present, detecting letters in distractor shapes and speech in noise, and picking up on semantic associations between unrelated words. Results using resting state functional MRI data suggested positive schizotypy, openness, and especially their shared variance, were related positively to connectivity of the default network and negatively to frontoparietal connectivity. Discussion Taken together, these findings suggest that pattern sensitivity and associated brain networks may underlie openness, positive schizotypy, and psychotic-like experiences. Those with heightened openness and associated risk for psychosis may demonstrate an increased default-network-related tendency toward erroneous thoughts and perceptions (false positives), coupled with diminished frontoparietal function and impairments in the ability to successfully engage in reality testing and screen out false positives. Overall, our results advance understanding of the personality and neurocognitive correlates of the extended psychosis phenotype, while adding to a growing body of research characterizing the underlying biology of transdiagnostic psychiatric features through the use of large, nonpatient samples.