What are the underlying neurocognitive mechanisms that give rise to mathematical competence? This study investigated the relationship between tests of mathematical ability completed outside the scanner and resting-state functional connectivity (FC) of cytoarchitectonically defined subdivisions of the parietal cortex in adults. These parietal areas are also involved in executive functions (EFs). Therefore, it remains unclear whether there are unique networks for mathematical processing. We investigate the neural networks for mathematical cognition and three measures of EF using resting-state fMRI data collected from 51 healthy adults. Using 10 ROIs in seed to whole-brain voxel-wise analyses, the results showed that arithmetical ability was correlated with FC between the right anterior intraparietal sulcus (hIP1) and the left supramarginal gyrus and between the right posterior intraparietal sulcus (hIP3) and the left middle frontal gyrus and the right premotor cortex. The connection between the posterior portion of the left angular gyrus and the left inferior frontal gyrus was also correlated with mathematical ability. Covariates of EF eliminated connectivity patterns with nodes in inferior frontal gyrus, angular gyrus, and middle frontal gyrus, suggesting neural overlap. Controlling for EF, we found unique connections correlated with mathematical ability between the right hIP1 and the left supramarginal gyrus and between hIP3 bilaterally to premotor cortex bilaterally. This is partly in line with the “mapping hypothesis” of numerical cognition in which the right intraparietal sulcus subserves nonsymbolic number processing and connects to the left parietal cortex, responsible for calculation procedures. We show that FC within this circuitry is a significant predictor of math ability in adulthood.