This study investigated the signaling pathways utilized by CB1 cannabinoid receptors (CB1R) to regulate neuronal Focal Adhesion Kinase (FAK) tyrosine phosphorylation (Tyr‐P) in murine N18TG2 cells. Immunoblotting experiments revealed the CB1R agonist WIN55212‐2 (WIN, 10 nM), produces three distinct phases of FAK Tyr‐P: Phase I (0–5 min) involves maximal Tyr‐P, Phase II (5–20 min) involves a decline in Tyr‐P, and Phase III (> 20 min) involves a plateau in Tyr‐P at submaximal levels. Phase I was blocked by the CB1R antagonist SR141716A and pertussis toxin which suggests maximal FAK Tyr‐P is mediated by CB1Rs and Gi/o proteins. The Src kinase inhibitor PP2 abolished Phase I which indicates Src is an absolute requirement for CB1R‐mediated maximal FAK Tyr‐P. Phase I also involved CB1R‐mediated transactivation of the Flk‐1 vascular endothelial growth factor receptor (Flk‐1 VEGFR). WIN induced Flk‐1 VEGFR Tyr‐P during Phase I, while Phase I was inhibited by the Flk‐1 VEGFR antagonist SU5416. The integrin receptor antagonist RGDS peptide also inhibited Phase I FAK Tyr‐P, while Cytochalasin D abolished Phase I FAK Tyr‐P which indicates dependence on an intact actin cytoskeleton and focal adhesions. WIN induced FAK association with β‐actin and the p85 subunit of phosphatidylinositol 3‐kinase during Phase I, as well as Protein Kinase B/Akt phosphorylation at Serine 473. These studies have identified a novel signaling pathway that mediates CB1R‐stimulated FAK Tyr‐P in neurons. Supported by NIDA grants R01DA003690 (ACH) and F32DA026295 (GDD).