Mammalian viruses transmit by hitch-hiking on the normal environmental sampling and social interactions of their hosts. Herpesviruses have colonized mammals since their earliest origins, suggesting that their entry mechanisms are likely to exploit ancient, common pathways. Yet these pathways remain ill-defined. Cytomegaloviruses (CMVs) are often assumed to enter new hosts orally, but sporadic transmission and late clinical presentation make early infection hard to track. Using live imaging, we show that Murine CMV (MCMV) infects mice nasally rather than orally, both after experimental inoculation and during natural transmission. Despite limited local replication, infection spread rapidly to systemic sites. The viral tropism determinant MCK2 promoted salivary gland colonization after nasal entry. However it was was redundant for entry itself. Tracking replication-deficient virions identified the primary target cells as olfactory neurons. Thus, MCMV exploited olfaction to enter new hosts.