Interest in the role of genetics in influencing key life outcomes such as educational attainment has grown quickly. However, the question of whether genetic influences on educational attainment, on average as well as in conjunction with socioeconomic circumstances, are moderated by macro-level factors has not yet received sufficient attention. This study combines polygenic indices for educational attainment (EA PGI) with high-quality register data in a large sample of Swedish twins of European ancestry born 1920–1999. Employing both conventional between-family and within-family models, the analyses suggest that the influences of education-related genetic propensities on educational attainment have increased in Sweden during the twentieth century, a period featuring major expansions of the Swedish educational system, and decreasing economic inequality. The analyses also suggest that the degree to which socioeconomic background enhances genetic influences on education has decreased across cohorts. Genetic influences on education do not appear to have translated into increased genetic influences on income. Additionally, there is some evidence of floor and ceiling effects in the analyses of dichotomous educational outcomes.