A diagnosis of epilepsy has significant consequences for an individual but is often challenging in clinical practice. Novel biomarkers are thus greatly needed. Here, we investigated how common genetic factors (epilepsy polygenic risk scores, [PRSs]) influence epilepsy risk in detailed longitudinal electronic health records (EHRs) of > 360k Finns spanning up to 50 years of individuals' lifetimes. Individuals with a high genetic generalized epilepsy PRS (PRSGGE) in FinnGen had an increased risk for genetic generalized epilepsy (GGE) (hazard ratio [HR] 1.55 per PRSGGE standard deviation [SD]) across their lifetime and after unspecified seizure events. Effect sizes of epilepsy PRSs were comparable to effect sizes in clinically curated data supporting our EHR-derived epilepsy diagnoses. Within 10 years after an unspecified seizure, the GGE rate was 37% when PRSGGE > 2 SD compared to 5.6% when PRSGGE < -2 SD. The effect of PRSGGE was even larger on GGE subtypes of idiopathic generalized epilepsy (IGE) (HR 2.1 per SD PRSGGE). We further report significantly larger effects of PRSGGE on epilepsy in females and in younger age groups. Analogously, we found significant but more modest focal epilepsy PRS burden associated with non-acquired focal epilepsy (NAFE). We found PRSGGE specifically associated with GGE in comparison with >2000 independent diseases while PRSNAFE was also associated with other diseases than NAFE such as back pain. Here, we show that epilepsy specific PRSs have good discriminative ability after a first seizure event i.e. in circumstances where the prior probability of epilepsy is high outlining a potential to serve as biomarkers for an epilepsy diagnosis.