Macrophages are sentinel innate immune cells, whose cytokine response drives effective host defence against influenza A virus (IAV). Macrophages can be directly infected by IAV, and sense viral RNA, proteins or virus-induced cellular perturbations by pattern recognition receptors expressed in strategic subcellular locations. The current dogma holds that the cell surface and endosomal toll-like receptors (TLR) 4,7,8 sense incoming IAV virions in dendritic cells and macrophages to drive pro-inflammatory and anti-viral cytokine expression, while the ubiquitously expressed, cytosolic retinoic acid-inducible receptor (RIG-I) detects IAV replication intermediates to drive anti-viral responses. Here we show that IAV pH1N1 (Auck09) abortively infects primary human monocyte derived macrophages (HMDM) and triggers a potent anti-viral (IFNB1, CXCL10) and pro-inflammatory (IL6, TNF) gene expression program. In contrast to published literature, the IAV polymerase inhibitor baloxivir marboxil blocked IAV-induced cytokine responses in HMDM, indicating that incoming virions are not sensed by cell-surface or endosomal receptors, and that HMDM sense replicating IAV virions. Consistent with this observation, TLR4 and TLR7/8 were dispensable for IAV-induced cytokine responses in HMDM. Using CRISPR/Cas9 to deplete RIG-I from HMDM, we confirmed that RIG-I sensing is critical for IAV-induced cytokine responses at 6 hours post infection, but not at 24h. In contrast, when we depleted mitochondrial antiviral signalling protein (MAVS), the shared adaptor for both RIG-I and the dsRNA sensor melanoma differentiation-associated factor 5 (MDA-5), we observed a complete loss of IAV-induced cytokine responses at 24hpi. This indicates another RLR, likely MDA-5 senses an unknown RNA ligand of virus or host origin to trigger a second wave of cytokine responses in human macrophages. Together, our data suggest that macrophages use alternate mechanisms of sensing to drive cytokine responses to IAV infection. Uncovering this receptor may identify new targets for improving protecting immunity to IAV or dampening pathological inflammation during severe IAV infection.