Introduction: Fibroblast activating protein (FAP) can be targeted on PET scan (FAPI-PET/CT) to detect small foci of pancreatic ductal adenocarcinoma (PDAC). Despite potential use in early diagnosis, little is known about FAP expression in the early stages of PDAC tumorigenesis. Methods: We performed immunohistochemistry against FAP on tumour microarrays of human intraductal papillary mucinous neoplasm with low-grade dysplasia (LGD; n=13), high-grade dysplasia (HGD; n=11), stage I PDAC (n=25), stage II-IV PDAC (n=50) and chronic pancreatitis (CP; n=48). We measured stromal and epithelial FAP expression, and compared this between benign (LGD, CP) and malignant pathology (HGD, Stage I, Stage II-IV PDAC). We also recruited patients with pancreatic cystic neoplasm (PCN; n=5) to undergo FAPI-PET/CT and monitored progress for 18 months. Results: All groups of malignant neoplasia had higher total FAP expression than LGD and CP (median: LGD=4; CP=4; HGD=8, Stage I=7; Stage II-IV=7; P<0.05 for all bivariate comparisons). Each malignant group had higher odds of positive FAP expression than LGD (OR[95% CI]: HGD=7.2[1.23-62.0]; Stage I=18.4 [3.44-151]; Stage II-IV=14.4[3.57-67.6]) and CP (HGD=2.34[0.51-16.9]; Stage I=5.98 [1.45-40.9]; Stage II-IV=4.68[1.57-16.0]). Expression was primarily epithelial if present in LGD, stromal in CP, and on both cell types in malignant neoplasia. Focal avidity on FAPI-PET/CT was observed in 3 cases of PCN, and these were the same 3 to later show malignant features. Conclusion: The transition to malignant dysplasia in the pancreas is marked by changes in FAP, both in the amount of expression and cell type involved. This can be detected on FAPI-PET/CT and may facilitate diagnosis of PDAC at a curable stage.