Genetic variation at variable number tandem repeat (VNTR) markers was used to assess population structure and diversity among 296 Fusarium graminearum isolates from northern Europe (Finland, northwestern Russia, and Norway), southern Europe (southwestern and western Russia), and Asia (Siberia and the Russian Far East). We identified at least two highly differentiated and geographically structured genetic populations (E1 and E2) in Eurasia (ΦPT = 0.35). Isolates from northern Europe were almost exclusively from the E1 population (95.6%) and had the 3ADON (3-acetyldeoxynivalenol) trichothecene genotype (97.3%). In contrast, all isolates from southern Europe were from the E2 population and 94.4% had the 15ADON (15-acetyldeoxynivalenol) genotype. The E2 population also predominated in the Asian sampling locations (92.7%) where 3ADON and 15ADON genotypes occurred at nearly equal frequencies. Southern European isolates were more closely related to those from Asia (ΦPT = 0.06) than to geographically closer populations from northern Europe (ΦPT ≥ 0.31). Northern European populations also harbored substantially less genetic diversity (Ne ≤ 2.1) than populations in southern Europe or Asia (Ne ≥ 3.4), indicative of a selective sweep or recent introduction and subsequent range expansion in northern Europe. Bayesian analyses incorporating previously described genetic populations from North America (NA1 and NA2) surprisingly identified NA2 and E2 as a single genetic population, consistent with hypotheses of a recent Eurasian origin for NA2. Additionally, more than 10% of the isolates from Asia and southern Europe were assigned to the NA1 population, indicating recent introductions of NA1 into parts of Eurasia. Collectively, these results demonstrate that there are at least three genetic populations of F. graminearum in the Northern Hemisphere and indicate that population-level diversity in Eurasia and North America has been shaped by recent transcontinental introductions.