Education is a major source of inequality in income and health. Polygenic indices for educational attainment (EA-PGI) capture both direct and indirect genetic influences on education, but their effects on income and health trajectories remain unclear. Using Finnish registry data on 51,056 genotyped graduates followed annually since graduation for up to 25 years, we report three findings. First, higher EA-PGI strongly predicts income growth, but only among higher-educated people: tertiary-educated graduates at the 90th percentile of EA-PGI distribution earn €45,392 (14 % of median) higher cumulated lifetime income than those at the 10th percentile. This effect is not mediated by overall health. Second, EA-PGI does not predict income differences at labor market entry or the quality of the first employer, but rather a higher job-to-job mobility toward better-paying firms, which drives the long-run income divergence. Third, controlling for parental EA-PGI in 12,871 parent–offspring trios reduces the cumulated lifetime income gap by 71 %, and the effect of paternal (but not maternal) EA-PGI on offspring income exceeds that of the offspring’s own EA-PGI. These findings suggest that genetic factors associated with educational attainment predict income trajectories primarily through faster and more frequent changes to higher-paying employers. However, much of this association reflects indirect paternal genetic effects, consistent with enduring paternal patterns of intergenerational job and income transmission.