A major goal of HIV-1 vaccine development is the elicitation of broadly neutralizing antibodies (bNAbs). During HIV-1 infection, such bNAbs arise as the result of a coevolutionary process between affinity maturing B cells and the escaping viral envelope (Env). To understand the ontogeny of bNAb lineages, and thus inform vaccine design strategies, we characterized antibody responses in 122 rhesus macaques (RMs) infected by 1 of 16 chimeric simian-human immunodeficiency viruses (SHIVs) bearing primary HIV-1 Envs. We isolated novel bNAbs targeting the Env V2 apex from ten of these RMs, and characterized their structures, immunogenetics, and developmental pathways. Structural analysis of these lineages showed recapitulation of the major modes of epitope recognition by human V2 apex bNAbs. Inference of bNAb precursors showed that they shared rare immunogenetic features with their mature counterparts, identifying precise requirements for priming. However, once primed, antibody lineage tracing revealed permissive maturation pathways associated with Envs that contained few escape mutations. Furthermore, epitope-specific Env escape was a sensitive indicator of apex-targeted responses that was absent in most macaques without bNAbs. To test the hypothesis that priming is the principal bottleneck to V2 apex bNAb elicitation during infection, we immunized a knock-in mouse model bearing the germline-reverted ancestor of one of these lineages and showed that bNAbs could be elicited by priming alone. Finally, we leveraged this information to engineer novel immunogens capable of eliciting antibodies to the V2 apex in humanized mice and RMs. These findings contribute to HIV-1 vaccine design by validating the RM model for studying V2 apex bNAb elicitation, identifying determinants of V2 apex bNAb elicitation during infection, establishing novel techniques for immunogen design and assessment, and providing novel immunogens for V2 apex bNAb elicitation.