Cells are enclosed by a membrane bilayer comprised of lipids and proteins. These membranes function to separate the extracellular environment from the internal cellular processes. Membrane proteins perform a wide variety of functions in the human cell. Most membrane proteins are synthesized at the endoplasmic reticulum (ER) membrane, where their transmembrane domains (TMDs) are inserted into the bilayer for subsequent folding and assembly. The GEL, PAT and BOS complexes have recently been defined as components of the “multipass translocon” (MPT) that coordinate with Sec61 to facilitate biogenesis of most metazoan multipass membrane proteins at the ER. In many cases, these multipass proteins also require the OST complex during synthesis, but how this is coordinated has only been explored for a small number of proteins. Here we present bioinformatic and biochemical analysis of the recruitment of both complexes to reveal how their access to the translocon is coordinated during protein synthesis. We utilize ultra-low input selective ribosome profiling to identify the co-translational clients of the MPT and OST. We find that the MPT subunits enrich for the same transcripts, and their recruitment is coordinated. The MPT is recruited during insertion of multiple TMDs. Some transcripts enriched by the MPT are also enriched by OST. Analysis of these footprints suggest that the MPT and OST respond to the opening and closing of the Sec61 channel, as dictated by the biophysical and topological requirements of the nascent chain. Overall, this work highlights the dynamic nature of the translocon during membrane protein biogenesis.