Given the essential role played by protein kinases in regulating cellular pathways, their dysregulation can result in the onset and/or progression of various human diseases. Structural analysis of diverse protein kinases suggests that these proteins exhibit a remarkable plasticity that allows them to adopt distinct conformations in response to interactions with other proteins, providing an opportunity for designing allosteric modulators. The present work reports the results of an in silico screening study aimed at identifying novel prospective allosteric binding sites in the paradigmatic p38α MAP kinase. The process was carried out using a protein ensemble generated from a 6 μs accelerated molecular dynamics simulation. The results of this calculation were first used to study the flexibility of the protein using Principal Component Analysis, followed by a Cluster Analysis aimed at producing an ensemble of conformations representative of the sampling process. Representative structures of the diverse clusters were subsequently screened for hot spots using FTMAP. The procedure permitted the identification of diverse allosteric sites of p38α already described in the literature including the DFG pocket, the lipid binding pocket, the DEF site, the docking groove, the CD and ED sites, and the backside site as well as a novel site recently reported: the A-loop regulatory site. Furthermore, the study also permitted the identification of ten novel prospective allosteric sites named NP1 to NP10, involving in most of the cases protein structural elements that control kinase activation including the activation loop, the catalytic loop, the αC helix, the L16 loop, and the glycine-rich loop.