The primary cilium is a central signaling component during embryonic development. Here we focus on CROCCP2, a hominid-specific gene duplicate from ciliary rootlet coiled coil (CROCC), also known as rootletin, that encodes the major component of the ciliary rootlet. We find that CROCCP2 is highly expressed in the human fetal brain and not in other primate species. CROCCP2 gain of function in the mouse embryonic cortex and human cortical cells and organoids results in decreased ciliogenesis and increased cortical progenitor amplification, particularly basal progenitors. CROCCP2 decreases ciliary dynamics by inhibition of the IFT20 ciliary trafficking protein, which then impacts neurogenesis through increased mTOR signaling. Loss of function of CROCCP2 in human cortical cells and organoids leads to increased ciliogenesis, decreased mTOR signaling, and impaired basal progenitor amplification. These data identify CROCCP2 as a human-specific modifier of cortical neurogenesis that acts through modulation of ciliary dynamics and mTOR signaling. Display omitted •CROCCP2: a hominid-specific gene duplicate uniquely expressed in human fetal cortex•CROCCP2 overexpression in the mouse embryo leads to cortical progenitor amplification•CROCCP2 is required for basal progenitor amplification in human cortical organoids•CROCCP2 acts by decreasing ciliogenesis and enhancing the mTOR pathway van Heurck et al. identify CROCCP2, a hominid-specific gene duplicate, as a human-specific modifier of neurogenesis in the developing cerebral cortex. They find that CROCCP2 is necessary and sufficient to enhance human cortical progenitor amplification and acts by decreasing primary cilia dynamics and enhancing the mTOR pathway.