Reelin is a large, secreted glycoprotein that is best known as an essential molecule directing neocortical neuronal migration, but reelin serves an important functional role in regulating neurite outgrowth and arborization as well. Canonically, reelin signals through the lipoprotein receptors apolipoprotein E receptor 2 (ApoER2) and very low-density lipoprotein receptor (VLDLR). Reelin can signal through non-canonical receptors and unidentified co-receptors as well, but the downstream effects of these non-canonical pathways are not well understood. Using an unbiased Tandem Mass Tag LC-MS/MS (TMT) proteomics screen and gene set enrichment analysis (GSEA), we identified overlapping and distinct intra-cellular pathways enriched downstream of canonical and non-canonical reelin signaling in primary murine neurons during periods of robust neurite arborization. We observed canonical signaling led to substantial changes in actin cytoskeletal dynamics and cell morphogenesis while non-canonical signaling preferentially regulated protein translation, suggesting reelin fine tunes neuronal structure and function through distinct signaling pathways. We also identified a novel node downstream of canonical reelin signaling, glycolytic enzyme and actin binding protein aldolase A (aldo A). Biochemical analysis revealed aldo A undergoes de novo translation and is dissociated from the actin cytoskeleton after acute reelin stimulation. Additionally, shRNA knockdown of aldo A in primary murine cultures and in vivo through in utero electroporation (IUE), reveal aldo A is necessary for reelin mediated neurite growth and the proper arborization and positioning of excitatory layer II/III neurons independent of glycolytic function. These results shed new light on the molecular mechanisms and signaling pathways regulating reelin dependent neuronal arborization.