Further exploration of viral-host cell interactions is crucial as we expand our understanding of influenza A virus (IAV) infection. Glycosylation is an often under-appreciated aspect of particular importance underlying these interactions, but a comprehensive understanding of how IAV infection shapes the host glycoproteome and the implications of these changes has yet to be attained. Using a liquid chromatography-tandem mass spectrometry (LC-MS/MS) approach, we performed proteomic, glycomic, and glycoproteomic characterisation of the dynamic subcellular responses in an in vitro time course infection of human A549 cells with two IAV strains (A/X-31, H3N2; A/Puerto Rico/8/1934, H1N1). We demonstrate that although infection resulted in relatively modest changes to the subcellular proteome, both H1N1 and H3N2 strains induced a robust and significant global reduction in the sialic acid content of both host secreted and intracellular membrane glycoproteins, and an increased abundance of oligomannose type glycosylation. Whilst the reduction in sialic acid consistent with the enzymatic activity of NA was observed globally across the glycoproteome, specific factors at both the glycan and protein level controlled the extent of desialylation. These data provide important insights into the host glycoproteome during influenza virus infection, furthering our understanding of viral-host interactions.