Background: Static [¹⁸F]FDG-PET/CT is the imaging method of choice for the evaluation of indeterminate lung lesions and NSCLC staging; however, histological confirmation of PET-positive lesions is needed in most cases due to its limited specificity. Therefore, we aimed to evaluate the diagnostic performance of additional dynamic whole-body PET. Methods: A total of 34 consecutive patients with indeterminate pulmonary lesions were enrolled in this prospective trial. All patients underwent static (60 min p.i.) and dynamic (0–60 min p.i.) whole-body [¹⁸F]FDG-PET/CT (300 MBq) using the multi-bed-multi-timepoint technique (Siemens mCT FlowMotion). Histology and follow-up served as ground truth. Kinetic modeling factors were calculated using a two-compartment linear Patlak model (FDG influx rate constant = Ki, metabolic rate = MR-FDG, distribution volume = DV-FDG) and compared to SUV using ROC analysis. Results: MR-FDG_mean provided the best discriminatory power between benign and malignant lung lesions with an AUC of 0.887. The AUC of DV-FDG_mean (0.818) and SUV_mean (0.827) was non-significantly lower. For LNM, the AUCs for MR-FDG_mean (0.987) and SUV_mean (0.993) were comparable. Moreover, the DV-FDG_mean in liver metastases was three times higher than in bone or lung metastases. Conclusions: Metabolic rate quantification was shown to be a reliable method to detect malignant lung tumors, LNM, and distant metastases at least as accurately as the established SUV or dual-time-point PET scans.