Developmental dyscalculia is a specific learning disorder that persists over lifetime and can have an enormous impact on personal, health-related, and professional aspects of life. Despite its central importance, the origin both at the cognitive and neural level is not yet well understood. Several classification schemas of dyscalculia have been proposed, sometimes together with an associated deficit at the neural level. However, these explanations are (a) not providing an exhaustive framework that is at levels with the observed complexity of developmental dyscalculia at the behavioral level and (b) are largely mono-causal approaches focusing on gray matter deficits. We suggest that number processing is instead the result of context-dependent interaction of two anatomically largely separate, distributed but overlapping networks that function/cooperate in a closely integrated fashion. The proposed two-network framework (TNF) is the result of a series of studies in adults on the neural correlates underlying magnitude processing and arithmetic fact retrieval, which comprised neurofunctional imaging of various numerical tasks, the application of probabilistic fiber tracking to obtain well-defined connections, and the validation and modification of these results using disconnectome mapping in acute stroke patients. Emerged from data in adults, it represents the endpoint of the acquisition and use of mathematical competencies in adults. Yet, we argue that its main characteristics should already emerge earlier during development. Based on this TNF, we develop a classification schema of phenomenological subtypes and their underlying neural origin that we evaluate against existing propositions and the available empirical data.