Many viruses, including HIV, mumps, Zika and SARS, infect the testis and disrupt fertility. This has been attributed to an inability of spermatogenic cells to produce anti-viral interferons (IFN) or IFN-induced proteins. Challenging this dogma, we discovered that interferon-epsilon (IFNe), a type-I IFN first identified in female reproductive epithelia, is constitutively expressed by meiotic and post-meiotic spermatogenic cells and testicular macrophages in mice and humans. We investigated the anti-viral role of IFNe in the testis, using an established mouse model of Zika virus infection and a human Sertoli cell-line (HSerc, ScienCellTM). Adult wildtype mice (WT), Ifne-/- mice lacking IFNe, and Ifnar1-/- mice lacking the IFNAR1 receptor subunit required for IFN-signalling, received a single intraperitoneal injection of Zika virus (PRVABC59, 5x105 pfu in saline). Controls received saline only. Reproductive organs were collected 7 days post-infection (peak illness). Infected WT mice lacked histological evidence of orchitis or epididymitis, but infected Ifne-/- and Ifnar1-/- mice displayed testicular hyperaemia, oedema and immune cell infiltrates. The epididymis of infected Ifne-/- mice displayed immune cell infiltrates, epithelial damage, luminal obstruction and fibrosis. Expression of critical Leydig cell (Cyp11a1, Cyp17a1) and spermatid genes (Tnp1) was also reduced in infected Ifne-/- and Ifnar1-/- mice. The human Sertoli cell-line was infected with 5 or 10 MOI Zika virus, and treated with 100IU recombinant human IFNe either 12h before or 1h after infection. qPCR for viral RNA and plaque assays for infectious virus performed 24h post-infection showed that IFNe pre-treatment reduced the viral load by ~98%. Post-infection IFNe treatment reduced viral RNA by ~70% and infectious virus by 97%. These data indicate that IFNe plays a key role in protecting the testis against Zika virus, shifting the existing paradigm of testicular anti-viral defences, and identifying IFNe as a potential therapeutic and diagnostic target in male reproductive tract infection and infertility.