Herpesviruses have co-evolved with their hosts over hundreds of millions of years, and exploit fundamental features of their biology.  Cytomegaloviruses (CMVs) colonize blood-borne myeloid cells and it has been hypothesized that systemic dissemination arises from infected stem cells in the bone marrow.  However, poor CMV transfer by stem cell transplantation argues against this being the main reservoir.  To identify alternative pathways for CMV spread, we tracked Murine CMV (MCMV) colonisation after mucosal entry.  We show that following intranasal MCMV infection, lung CD11c⁺ dendritic cells (DC) migrated sequentially to lymph nodes (LN), blood, then salivary glands.  Replication-deficient virus followed the same route and thus DC infected peripherally traversed LN to enter the blood.  Given that DCs are thought to die locally following their arrival and integration into LN, recirculation to the blood represents a new pathway.  We examined host and viral factors that facilitated this LN traverse.  We show that MCMV-infected DC exited LN by a distinct route to lymphocytes, entering high endothelial venules and bypassing the efferent lymph.  LN exit required CD44 and the viral M33 chemokine receptor, without which infected DC accumulated in LN and systemic spread was greatly reduced.  Taken together, our studies provide the first demonstration of viral-driven DC recirculation.  As viruses follow host-defined pathways, high endothelial venules may normally allow DC to pass from LN back to the blood.