Human cytomegalovirus (HCMV) has a tremendous coding capacity within its dsDNA genome that has allowed it to coevolve with its host. Transcription of the virus genome is not limited to protein-coding genes; in fact, most of the transcription from the HCMV genome during lytic replication generates viral ncRNAs that are not translated into protein. Four long ncRNAs (RNA5.0, RNA4.9, RNA1.2 and RNA2.7) account for the majority of HCMV transcription during lytic replication. Here, we review the expression and function of these long ncRNAs in the context of virus replication and pathogenesis. Long ncRNAs may contribute to HCMV evasion of the host response and manipulate cellular and viral programs to successfully persist throughout the lifetime of its host.