Alzheimer's disease (AD) arises from heterogeneous biological processes, and long-term environmental exposures may become biologically embedded, as reflected in epigenetic clocks. We calculated blood DNA methylation-based epigenetic clocks and constructed protein co-abundance networks of cerebrospinal fluid (CSF) proteomics data. We performed association analysis of epigenetic age acceleration with network modules, followed by functional and cell-type enrichment analyses, association analyses of hub proteins with AD endophenotypes, and pseudotime trajectory analysis. Six network modules were significantly associated with epigenetic age acceleration and were enriched in pathways related to neuronal connectivity, proteostasis, immune activation and remodeling, immune signaling, and immunoepigenetic regulation. Hub proteins demonstrated significant associations with baseline amyloid/tau/neurodegeneration biomarkers and longitudinal cognitive changes. Pseudotime analysis revealed continuous, non-linear variation in epigenetic age acceleration along the inferred trajectory. Our CSF proteomics study identified neuronal, proteostatic, and immune-related molecular signatures associated with epigenetic age acceleration in AD.