An innovative biomaterial is needed to improve the tissue response and treatment outcomes in vital pulp tissue. In this regard, proanthocyanidins (PAs) have the potential to be used as a bioactive content of a scaffold since they can regulate oxidative stress and induce mineralization. The aim of this study was to engineer biodegradable electrospun polymeric nanofibers (Nfs) to enable the sustained release of PAs through a β-cyclodextrin (β-CD) inclusion complex and to investigate the effects of Nf mats on viability and the odontogenic differentiation capability of dental pulp stem cells (DPSCs). Bare polylactic acid nanofibers (PLA-Nfs), as well as 75 μg/mL PA-incorporated PLA_PA-Nf, and PLA-IC-Nf mats, were fabricated through the electrospinning technique. The morphology, composition, and hydrophilicity of the Nfs were characterized by scanning electron microscopy, attenuated total reflection Fourier transform infrared spectroscopy, and contact angle measurements, respectively. The release of PA from the fibers was monitored for 30 days at predetermined intervals. The inclusion complex enabled the electrospun PLA-IC-Nfs to demonstrate a more sustained release profile of PA compared to that of the PLA_PA-Nfs. The antioxidant capacity was evaluated using the 2,2-diphenyl-1-picrylhydrazyl assay, and the antibacterial effects against Staphylococcus aureus and Escherichia coli were investigated by counting the colony-forming units. To assess odontogenic differentiation; calcium deposition and alkaline phosphatase (ALP) activity, Alizarin red staining was measured on day 14 and 18, while the levels of expression of the osteocalcin, Runt-related transcription factor 2, dentin sialophosphoprotein (DSPP), and dentin matrix protein (DMP) genes were evaluated on day 18. As a result, the successfully developed PLA-IC-Nf exhibited effective antibacterial activity against S. aureus and E. coli, antioxidant activity, and increased hydrophilicity compared to Nfs without the inclusion complex. Although the PLA-IC-Nf showed initial cytotoxicity, it gradually decreased over time to levels comparable with those of DPSCs alone, allowing the cell culture to reestablish itself due to a more controlled release. PLA-IC-Nf samples promoted odontogenic differentiation of DPSCs by upregulating the DSPP, DMP-1, and ALP activity.