The cerebral cortex has expanded during recent human evolution, resulting in complex neural circuits for higher cognitive abilities that characterise our species. The molecular and cellular mechanisms behind human cortical evolution are largely unknown, in part due to the difficulty of direct observation and experimental perturbation in vivo. Recent technical advances in modeling human cortical development in vitro have opened the way to uncovering human uniqueness in the molecular and cellular mechanisms leading to massive cortical elaboration. We have developed a long-term recording system to monitor the behaviour of neural progenitors during early cortical neurogenesis at single-cell resolution. Using this system, we have uncovered critical differences in progenitor dynamics between humans and chimpanzees that are highly relevant to the three-fold difference in cortical volume between the two species. Such species-specific developmental mechanisms must be controlled by species-specific molecular regulation. The most promising candidates are human-specific genes acquired in the recent human evolutionary lineage after the split from chimpanzees. We have compiled a comprehensive list of human-specific genes that arose through recent duplication of pre-existing genes and examined their expression dynamics during fetal cortical development. We and others have found that human-specific genes are involved in multiple processes of cortical development, from progenitor amplification to the establishment of synaptic connections between differentiated neurons. As an example, we present the cell biological mechanisms of cortical progenitor maintenance by the human-specific gene NOTCH2NL and the evolutionary tuning of this gene activity. We believe that the comprehensive functional evaluation of human-specific genes will reveal the critical species differences in the molecular and cellular mechanisms that underlie human uniqueness in brain development and function.