Epstein-Barr Virus infection of B lymphocytes elicits diverse host responses via well-adapted transcriptional control dynamics. Consequently, this host-pathogen interaction provides a powerful system to explore fundamental processes leading to consensus fate decisions. Here we use single-cell transcriptomics to construct a genome-wide multistate model of B cell fates upon EBV infection. Additional single-cell data from human tonsils revealed correspondence of model states to analogous in vivo phenotypes within secondary lymphoid tissue, including a previously uncharacterized EBV(+) analog of multipotent activated precursors that can yield early memory B cells. These resources yield exquisitely detailed perspectives of the transforming cellular landscape during an oncogenic viral infection that simulates antigen-induced B cell activation and differentiation. Thus, they support investigations of state-specific EBV-host dynamics, effector B cell fates, and lymphomagenesis. To demonstrate this potential, we identify EBV infection dynamics in FCRL4(+) / TBX21(+) atypical memory B cells that are pathogenically associated with numerous immune disorders.