HIV-1 is readily-detected in resting CD4+ T-cells in vivo1-4. However, resting T-cells are highly-refractory to cell-free virus infection in vitro5-7 and require mitogenic activation to become permissive. This paradox raises the fundamental question of what makes a T-cell permissive for HIV-1. Here we address this and show that HIV-1 capsid nuclear import at the nuclear pore complex (NPC) is a bottleneck to resting T-cell infection, but that HIV-1 overcomes this by triggering receptor-mediated signalling during cell-cell spread to drive nuclear import and licence infection. Coupling viral and cellular assays with super-resolution imaging we show that contact between HIV-1 infected and uninfected T-cells triggers CD4-Lck signalling that activates CDK1, independent of cell-cycle entry, phosphorylating nucleoporins and priming the NPC to promote HIV-1 nuclear import. Critically, cell-cell contact also accelerates nuclear import in activated T-cells, providing a new paradigm for why cell-cell spread dominates infection. By contrast, HIV-1 virions do not trigger this response, explaining why resting T-cells cannot be efficiently infected by cell-free virus. We propose that HIV-1 has evolved to activate CD4 signalling during cell-cell spread to regulate infection at the step of the NPC, thereby bypassing the need for T-cell activation and offering an explanation for how resting T-cells can be infected in vivo.