Pancreatic cancer is characterized by its aggressive metastatic nature and its resistance to common chemotherapy treatment with a dense, desmoplastic ECM that can both promote and prevent PDAC progression. The multifunctional protein FAK acts at the intersection of various signaling pathways often hijacked in cancer progression and metastasis and is a known regulator of ECM stiffness and mechano-signaling in both stromal and epithelial compartments. Here, we used intravital imaging in live tumors to visualize fine-tuned epithelial and stromal manipulation via FAK inhibitor (FAKi) priming to improve systemic chemotherapy whilst reducing metastatic spread in mouse and patient-derived PDAC models. Live tumor imaging of the FUCCI cell cycle reporter, in parallel with target validation via of FAK targeting via FRET-imaging of an FAK biosensor helped us to guide and optimize treatment response at both primary and secondary sites. Critically, fluid flow-induced shear-stress assessment and personalized patient-derived matrices also allowed us to deconstruct the benefits by which FAKi priming can reduce PDAC spread during disease progression and metastatic transit. Lastly, orthotopic stratification of PDAC patient samples from the Australian Pancreatic Genome Initiative (APGI) revealed a subset of patients that have poor prognosis and are likely to respond to FAKi priming regimens, where short-term stromal manipulation and epithelial FAK inhibition prior to chemotherapy may improve patient outcome and reduce the need for chronic combination therapy in PDAC.