For better translational outcomes researchers and clinicians alike demand novel tools to distil complex neuroimaging data into simple yet behaviorally relevant representations at the single-participant level. Recently, the Mapper approach from topological data analysis (TDA) has been successfully applied on noninvasive human neuroimaging data to characterize the entire dynamical landscape of whole-brain configurations at the individual level without requiring any spatiotemporal averaging at the outset. Despite promising results, initial applications of Mapper to neuroimaging data were constrained by (1) the need for dimensionality reduction, and (2) lack of a biologically grounded heuristic for efficiently exploring the vast parameter space. Here, we present a novel computational framework for Mapper—designed specifically for neuroimaging data—that removes limitations and reduces computational costs associated with dimensionality reduction and parameter exploration. We also introduce new meta-analytic approaches to better anchor Mapper-generated representations to neuroanatomy and behavior. Our new NeuMapper framework was developed and validated using multiple fMRI datasets where participants engaged in continuous multitask experiments that mimic “ongoing” cognition. Looking forward, we hope our framework could help researchers push the boundaries of psychiatric neuroimaging towards generating insights at the single-participant level while scaling across consortium-size datasets.