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After birth, the mammalian brain undergoes numerous molecular changes that underlie cognitive plasticity and maturation. However, little is known about the dynamics of three-dimensional (3D) genome structure during this period. Here we generated a 3D genome atlas of 1,954 single cells from the developing mouse cortex and hippocampus, using our diploid chromatin conformation capture (Dip-C) method. In adult tissues, genome structure alone delineates major cell types such as cortical excitatory and inhibitory neurons, and hippocampal granule cells. During development, a major transformation was observed between the first and fourth week after birth-coincident with synaptogenesis and de novo DNA methylation, leading to 3D reorganization across multiple genomic scales. Using reciprocal crosses, we systematically examined allele-specific structure of imprinted genes, revealing chromosome-wide difference at the Prader-Willi/Angelman syndrome locus. These findings thus uncover a previously unknown dimension of postnatal brain development.