Influenza A virus (IAV) infection initiates a high-stakes competition for proteostatic control. While the host reconfigures its degradative machinery for defense, the virus simultaneously hijacks host proteostatic and degradative pathways to facilitate replication and evade immunity. Central to this conflict is the proteasomal switch, a process in which constitutive proteasome subunits (β1, β2, β5) are replaced by their inducible counterparts (β1i, β2i, β5i) to form the immunoproteasome (iP). Although iP is classically recognized for optimizing MHC class I antigen presentation, emerging evidence reveals more nuanced roles in IAV infections. This review synthesizes current knowledge on iP as an effector of host defense and target for viral subversion. We synthesize emerging evidence and propose working models detailing how IAV proteins may selectively interfere with proteasomal subunits to stabilize pro-viral factors. Furthermore, we examine the hypothesis that the iP functions alongside broader ubiquitin-proteasome system (UPS), endoplasmic reticulum-associated degradation (ERAD), and autophagic pathways as a proteostatic buffer to mitigate proteotoxic and oxidative stress in the infected epithelium. By evaluating how age-related proteostatic decay and viral subversion could impair cellular clearance machinery, we provide a conceptual framework for understanding how proteasomal dysregulation contributes to acute lung injury and the chronic inflammatory state termed as inflammaging. Finally, we propose a hypothesis-generating, biphasic framework for timing-dependent proteasomal modulation, contrasting preclinically supported late-stage β5i inhibition against the theoretical concept of early-stage activation to highlight translational hurdles in severe influenza.