The initial steps of the human immunodeficiency virus 1 (HIV-1) lifecycle are regulated by cellular RNA-binding proteins (RBPs). However, the scope of these early host-virus interactions remain largely uncharecterised. To fill this gap, we developed in virion RNA interactome capture (ivRIC) to profile comprehensively and systematically the proteins that interact with the HIV-1 genomic (g)RNA inside viral particles. ivRIC identified 105 cellular RBPs within the encapsidated HIV-1 ribonucleoprotein, many of which are surprisingly nuclear. Analysis of the interactome of HIV-1 RBP Rev in infected cells revealed that most in virion incorporated (iv)RBPs likely associate with HIV-1 gRNA during its nuclear life. Functional assays showed that ivRBPs are important for HIV-1. For example, we found that PURA and PURB control viral gene expression and infectivity through interaction with critical sequences in the gRNA. In summary, the compositional analysis of the encapsidated ribonucleoprotein of HIV-1 uncovers host-virus interactions controlling virus infection.