The external environment influences brain cell proliferation, and this might contribute to brain plasticity underlying adaptive behavioural changes. Additionally, internal genetic factors influence brain cell proliferation rate. However, to date, researchers have not examined the importance of environmental vs. genetic factors in causing natural variation in brain cell proliferation. Here, we examine brain cell proliferation and brain growth trajectories in free-living populations of Trinidadian killifish, Rivulus hartii, exposed to contrasting predation environments. Compared to populations without predators, populations in high predation environments exhibited higher rates of brain cell proliferation and a steeper brain growth trajectory (relative to body size). To test whether these differences in the wild persist in a common garden environment, we reared first generation fish originating from both predation environments in uniform laboratory conditions. Just as in the wild, brain cell proliferation and brain growth in the common garden were greater in high predation populations than in no predation populations. The similar results in field and common garden studies indicate that population differences in these brain features are intrinsic, probably genetic, differences arising from natural selection acting on overall brain growth and life history rather than differences arising through phenotypic plasticity.