The precise origin of SARS-CoV-2 remains a pressing question in the global community yet little structural investigation has been done on its closest genetic relatives within the SARS-related coronavirus species (SARSr-CoV). We present three novel SARSr-CoV glycoprotein structures through single particle cryo-EM analysis derived from bat (bCoV-WIV1) and civet (cCoV-SZ3, cCoV-007) hosts at a resolution of 1.88 Å, 1.92 Å, and 2.10 Å, respectively. With the inclusion of these novel structures, we review the structural conservation of biologically relevant regions across the entire sarbecovirus subgenus. We describe heavy glycosylation with complex glycan trees of all three novel glycoproteins as well as identify water molecule coordination within structurally important regions. We compare this to the general glycosite patterns across the SARSr-CoV species and describe the difficulties faced when solving the glycan shields structurally. We note structural conservation across the subgenera of the fatty acid binding pocket (FABP) occupied by linoleic acid (EIC) when the receptor binding domain (RBD) is in the “down” conformation, and identify the occupied biliverdin binding pocket in the N-terminal domain (NTD), noting structural evidence in previously published glycoproteins which has not been addressed. Finally, we analysed structural differences in a loop of the receptor binding motif (RBM) between human infecting coronaviruses and animal coronaviruses, which may account for hACE2 binding. The disconnect between the genetic similarity found across the sarbecovirus subgenus and the structural evidence currently available is limiting our knowledge of these proteins and their effect in vivo. Identifying the conservation and variation in structure between human and animal coronaviruses can inform on the likelihood of future cross-species transmission, allowing us to prepare for potential zoonotic emergences and develop pan-neutralising treatments.