The brain extracellular matrix (ECM) provides a physical framework and biochemical milieu for early (embryonic) morphogenetic and later (fetal and neonatal) histogenetic events. The specific ECM constituents and their dynamic spatial and temporal distribution at transcriptomics and protein levels were researched using RNAseq analysis and immunohistochemistry in 200 postmortem fetal and postnatal human brains. The ECM is especially prominent in the transiently voluminous histogenetic zones such as the neocortical preplate, subplate, and marginal zone. Still, it is also present in the smaller developmental analogs, such as ECM of pre-subplate, indusium griseum, subcortical crossroads of pathways, callosal septa, and others, equally rich in the glycosaminoglycans' content during the mid-fetal period. While some of the ECM constituents have a role in the tangential organization of the telencephalic wall, like tenascins, fibronectin, and chondroitin-sulfate proteoglycans (PG), others have a role in regionalization, such as versican and keratan sulfate PG, or postnatally are involved in the specification of cortical microcircuitries, like brevican, aggrecan, neurocan via perineuronal net formation around the specific neuronal population. Postnatal reorganizations of these ECM-rich developmental telencephalic compartments extend into the second year of life. Developmental changes in the amount and composition of the ECM are significant for changes in magnetic resonance imaging signal intensity of the fetal and early postnatal human brain; therefore, knowledge of ECM-related developmental events is essential for diagnostic, prognostic, and therapeutic approaches in fetal and perinatal medicine.