Bone regeneration requires coordinated vascularization and microenvironmental remodeling; however, most bone biomaterials have primarily emphasized angiogenesis and have less explicitly addressed lymphatic-associated responses. Here, inspired by developmental bone formation and emerging evidence implicating the interleukin-6 (IL-6)–CXCL12 axis in regenerative processes, we developed a biomimetic platform to promote bone repair, accompanied by coordinated blood-vascular and lymphatic-associated responses. A 3D-printed Haversian-mimetic scaffold with architecturally defined microchannels was fabricated to support guided tissue infiltration and vascular organization. To provide instructive biochemical signaling, a gelatin methacrylate (GelMA)-based coating enabled sustained, low-dose delivery of IL-6. Developmental immunofluorescence analysis revealed pronounced spatial association between CXCL12 and osteocalcin-positive osteogenic regions, providing a biological rationale for engaging this axis as a regeneration-associated cue. In vitro studies demonstrated enhanced osteogenic differentiation and concomitant upregulation of angiogenic and lymphatic-associated markers. Transcriptomic profiling further indicated activation of gene programs associated with extracellular matrix remodeling, vascular-related signaling, and tissue regeneration. In a critical-sized defect model, the IL-6-functionalized Haversian-mimetic scaffold promoted new bone deposition and was accompanied by increased CD31-positive vascular structures, lymphatic vessel endothelial hyaluronan receptor 1 (LYVE1)-positive lymphatic-associated structures, and CXCL12 expression. Collectively, this work demonstrates a strategy that integrates architectural mimicry with cytokine signaling to enhance bone regeneration while explicitly evaluating lymphatic-associated responses as a design parameter for next-generation bone biomaterials.