BACKGROUND: Cerebral arteriovenous malformations (AVMs) are pathological connections between arteries and veins. Dual-venc 4D flow MRI, an extended 4D flow MRI method with improved velocity dynamic range, provides time-resolved 3D cerebral hemodynamics. PURPOSE: To optimize dual-venc 4D flow imaging parameters for AVM; to assess the relationship between spatial resolution, acceleration, and flow quantification accuracy; and to introduce and apply the flow distribution network graph (FDNG) paradigm for storing and analyzing complex neurovascular 4D flow data. STUDY TYPE: Retrospective cohort study. SUBJECTS/PHANTOM: Scans were performed in a specialized flow phantom: 26 healthy subjects (age 41 ± 17 years) and five AVM patients (age 27-68 years). FIELD STRENGTH/SEQUENCE: Dual-venc 4D flow with varying spatial resolution and acceleration factors were performed at 3T field strength. ASSESSMENT: Quantification accuracy was assessed in vitro by direct comparison to measured flow. FDNGs were used to quantify and compare flow, peak velocity (PV), and pulsatility index (PI) between healthy controls with various Circle of Willis (CoW) anatomy and AVM patients. STATISTICAL TESTS: In vitro measurements were compared to ground truth with Student's t-test. In vivo groups were compared with Wilcoxon rank-sum test and Kruskal-Wallis test. RESULTS: Flow was overestimated in all in vitro experiments, by an average 7.1 ± 1.4% for all measurement conditions. Error in flow measurement was significantly correlated with number of voxels across the channel (P = 3.11 × 10(-28) ) but not with acceleration factor (P = 0.74). For the venous-arterial PV and PI ratios, a significant difference was found between AVM nidal and extranidal circulation (P = 0.008 and 0.05, respectively), and between AVM nidal and healthy control circulation (P = 0.005 and 0.003, respectively). DATA CONCLUSION: Dual-venc 4D flow MRI and standardized FDNG analysis might be feasible in clinical applications. Venous-arterial ratios of PV and PI are proposed as network-based biomarkers characterizing AVM nidal hemodynamics. LEVEL OF EVIDENCE: 3 Technical Efficacy: Stage 1 J. Magn. Reson. Imaging 2019;50:1718-1730.