Parkinson’s Disease (PD) is a neurodegenerative disorder that affects dopamine-producing neurons in an area of the mid-brain called the substantia nigra. It is the second most commonly occurring neurogenerative disorder worldwide, following Alzheimer’s Disease. The exact mechanism behind the manifestation of PD remains widely unknown, a limitation that contributes to the lack of a cure for the disease. Over 8.5 million persons worldwide are affected by PD, and that number is expected to double within the next 20 years, making research into the understanding of Parkinson’s even more paramount to developing a cure. The most common type of PD is sporadic Parkinson’s, which accounts for 90% of the cases. In persons with sporadic Parkinson’s, the cause of the disease is unclear, and the progress is spontaneous. The other 10% of PD cases are caused by genetic mutations, with a vast majority of these subsets taking place in the Leucine-Rich-Repeat Protein Kinase-2 Domain (LRRK2). LRRK2 is a multidomain protein consisting of seven domains with both GTPase and kinase activity. Mutations within several domains along LRRK2 are linked to PD, resulting in hyperphosphorylation of LRRK2-activated downstream Rab GTPases, which result in cellular trafficking defects and a disruption of cellular homeostasis. In this research, we employ the use of constrained (stapled) peptides to inhibit protein-protein interactions (PPIs) at different domains along LRRK2 to turn off the downstream hyperphosphorylation associated with PD-related LRRK2 mutations. We synthesize constrained peptide mimics of the LRRK2 C-tail and the COR domain and hypothesize that the COR-COR dimerization and the C-tail interaction with the protein’s kinase domain energetically contribute to the activation of the LRRK2 pathway and may be a key target to inhibiting LRRK2 activity as it relates to PD. Further, we synthesized an additional library of constrained peptides that target LRRK2 substrates, Rab8a and RILPL2, to inhibit their PPI to directly downregulate cilia damage and centrosomal splitting, two key cellular defects associated with PD. Collectively, these three distinct constrained peptide libraries aid in characterizing this poorly understood PD-associated pathway while simultaneously offering an alternative approach to targeting and inhibiting the LRRK2 protein.