Focal adhesion kinase (FAK) is a protein tyrosine kinase that plays a major role in regulating cell adhesion, proliferation, motility, and survival. While FAK-regulatory phosphosites play significant roles in cancer progression and metastasis, the broader perspective of its phosphorylation remains largely unknown. Therefore, mapping the phosphoregulatory networks provides significant insights into targeted therapies. To characterize the phosphorylations of FAK, we systematically retrieved PubMed-indexed studies and compiled large-scale cellular mass spectrometry-based phosphoproteomics datasets. An integrative, data-driven analysis was performed on 678 qualitative and 235 quantitative cellular phosphoproteomic datasets to map the signatures of FAK phosphorylation. The study observed that the S910 modification is the most frequently detected phosphorylation outside the catalytic kinase domain. This predicts a broader regulatory role of S910 in signaling than previously understood. Further, by integrating phosphosite co-detection patterns across diverse biological contexts, we characterized FAK phosphorylations and their co-regulated Phosphosites in Other Proteins (PsOPs). The phospho-coregulatory analysis of S910 and FAK activation phosphosites Y576, Y577, and Y861 provided distinct potential phosphosite cross-talks. Furthermore, the study predicts several potential candidate substrates and interactor PsOPs, providing a framework for prioritizing phosphosites for future experimental investigation. Moreover, the study also illustrated a hypothesized model of potential FAK phosphosite-specific coregulatory associations within gastrin-associated signaling. Taken together, these large-scale observations provide a data-driven foundation for future FAK-centered experimental approaches and understanding of its multifaceted role as a potential target.