Promiscuous proteins are commonly observed in biological systems, for example, in modular domains that recognize phosphopeptides during signal transduction. This promiscuous recognition is of fundamental interest in chemistry and biology but is challenging when designing phosphopeptides in silico for cell biology studies. To investigate promiscuous recognition and binding processes of phosphopeptides and the modular domain, we selected a domain essential in breast cancer-the breast-cancer-associated protein 1 (BRCA1) C-terminal (BRCT) repeats as our model system. We performed molecular dynamics simulations and detailed analyses of the dihedral space to study protein fluctuation and conformational changes with phosphopeptide binding. We also studied the association processes of phosphorylated and unphosphorylated peptides using Brownian dynamics with a coarse-grained model. We found that the BRCT domain is preorganized for phosphopeptide binding but has a moderate arrangement of side chains to form complexes with various types of phosphopeptides. Phosphopeptide binding restricts the system motion in general, while the nonpolar phosphopeptide becomes more flexible in the bound state. Our analysis found that the BRCT domain utilizes different mechanisms, usually termed lock and key, induced-fit, and population-shift/conformational-selection models, to recognize peptides with different features. Brownian dynamics simulations revealed that the charged phosphate group may not always accelerate peptide association processes, but it helps the phosphopeptide orient into binding pockets accurately and stabilizes the complex. This work provides insights into molecular recognition in the promiscuous protein system.