The impact of natural selection on the adaptive divergence of invasive populations can be assessed by testing the null hypothesis that the extent of quantitative genetic differentiation (QST) would be similar to that of neutral molecular differentiation (FST). Using eight microsatellite loci and a common garden approach, we compared QST and FST among ten populations of an invasive species Ambrosia artemisiifolia (common ragweed) in France. In a common garden study with varying water and nutrient levels, we measured QST for five traits (height, total biomass, reproductive allocation, above- to belowground biomass ratio, and days to flowering). Although low FST indicated weak genetic structure and strong gene flow among populations, we found significant diversifying selection (QST > FST) for reproductive allocation that may be closely related to fitness. It suggests that abiotic conditions may have exerted selection pressure on A. artemisiifolia populations to differentiate adaptively, such that populations at higher altitude or latitude evolved greater reproductive allocation. As previous studies indicate multiple introductions from various source populations of A. artemisiifolia in North America, our results suggest that the admixture of introduced populations may have increased genetic diversity and additive genetic variance, and in turn, promoted the rapid evolution and adaptation of this invasive species.