The recent demographic transitions to lower mortality and fertility rates in most human societies have led to changes and even quick reversals in phenotypic selection pressures. This can only result in evolutionary change if the affected traits are heritable, but changes in environmental conditions may also lead to subsequent changes in the genetic variance and covariance (the G matrix) of traits. It currently remains unclear if there have been concomitant changes in the G matrix of life-history traits following the demographic transition. Using 300 years of genealogical data from Finland, we found that four key life-history traits were heritable both before and after the demographic transition. The estimated heritabilities allow a quantifiable genetic response to selection during both time periods, thus facilitating continued evolutionary change. Further, the G matrices remained largely stable but revealed a trend for an increased additive genetic variance and thus evolutionary potential of the population after the transition. Our results demonstrate the validity of predictions of evolutionary change in human populations even after the recent dramatic environmental change, and facilitate predictions of how our biology interacts with changing environments, with implications for global public health and demography.