Thylakoid membranes are highly dynamic structures that are essential for photosynthesis and particularly vulnerable to photo-oxidative stress. Although several factors involved in thylakoid biogenesis and maintenance have been identified, the molecular mechanisms that preserve membrane integrity under stress conditions remain poorly understood. In this study, we used mass spectrometry–based proteomics to identify protein complexes involved in chloroplast membrane stress responses. Guided by the chloroplast unfolded protein response (cpUPR), a stress signaling pathway that links chloroplast proteostasis to membrane remodeling, we focused on proteins upregulated in a MARS1-dependent manner during photo-oxidative stress in Chlamydomonas reinhardtii. FLAG immunoprecipitation coupled to mass spectrometry (IP–MS) was employed to characterize the interactome of VIA1 (VIPP1-Associated Protein 1), a conserved chloroplast protein identified as a cpUPR target, and to define its relationship with the thylakoid membrane remodeling factor VIPP1. A reciprocal IP–MS experiment using a polyclonal VIPP1 antibody was performed under control and high-light stress conditions to identify stress-dependent interactions and confirm the binding to VIA1. An additional VIPP1-IP experiment was conducted to assess the impact of targeted mutations that disrupt the VIA1–VIPP1 interaction. To evaluate evolutionary conservation, complementary FLAG-based IP–MS analyses were performed in Synechocystis sp. PCC 6803 expressing a tagged VIA1 ortholog. Together, these datasets define conserved stress-associated interaction networks centered on VIA1 and VIPP1 and provide proteomic evidence for a conserved membrane stress–response module operating across photosynthetic organisms.