Eukaryotic translation initiation requires the recruitment of the large, multiprotein eIF3 complex to the 40S ribosomal subunit. Using X-ray structures of all major components of the minimal, six-subunit Saccharomyces cerevisiae eIF3 core, together with cross-linking coupled to mass spectrometry, we were able to use IMP to position and orient all eIF3 components on the 40S•eIF1 complex, revealing an extended, modular arrangement of eIF3 subunits. For more information about how to reproduce this modeling, see https://salilab.org/40S-eIF1-eIF3 or the README file.