How neural circuits supporting human cognition evolved is a topic of enduring interest. The lack of tools available to map human brain circuits has precluded our ability to map the human connectome and trace its evolution. Here, we harness ultra-high resolution connectomic, anatomic, and transcriptomic variation to investigate the evolution and development of frontal cortex circuitry in humans. We align temporal trajectories in gene expression to identify equivalent ages across humans, macaques, and mice during postnatal development. We use these data to test for cross-species variation in developmental programs leading to modifications in adult neural circuits. We test for cross-species variation in temporal and spatial expression of genes linked to long-range projections across the frontal cortex (i.e., “supragranular-enriched genes”). We also compare the growth and pathway types coursing through the frontal cortex of mice, macaques, and humans with structural and high resolution diffusion MR tractography. We find that compared with that of mice, frontal cortex circuitry development is protracted in primates and is concomitant with an expansion of cortico-cortical projections in adulthood. We also find very little variation in these parameters among studied primates. For instance, an analysis of variance on the proportion of cortico-cortical pathways shows major differences across the three species (F=19.11; p<0.05; n=17) but post hoc Tukey tests show no differences between humans and macaques (p>0.05). These data together identify a collection of conserved features in frontal cortex circuitry of humans and Old World monkeys. Our work is the first to demonstrate that integrating transcriptional and connectomic data across temporal dimensions in primates is a robust approach to trace the evolution of human brain connectomics.