Genetic association data, immunohistochemistry, and functional experiments implicate protein arginine deiminase 4 (PAD4) in the pathogenesis of rheumatoid arthritis (RA). This disease is characterized by immunity against epitopes with deiminated arginine (=citrulline) originating from a multitude of intra-and extracellular proteins that are modified in this manner only in RA patients, not in healthy individuals. However, it remains uncertain how, where, and why PAD4 citrullinates these proteins in the RA patients. To gain insights into the physical interactions of PAD4 with other cellular proteins, we identified candidate PAD4-associated proteins by mass spectrometry. PAD4 in neutrophils from RA patients and healthy controls co-immunoprecipitated with myosin-9, and 20 other proteins, many of which were also present in myosin-9 immunoprecipitates. By immunofluorescence microscopy, PAD4 co-localized with myosin-9, myosin light chain 6, and other associated proteins in RA neutrophils. This was confirmed by proximity ligation assays in intact neutrophils. Inhibition of the motor domain of myosin-9 by blebbistatin resulted in a more diffuse PAD4 location indicating that myosin-9 serves to transport PAD4 within the cells. However, PAD4 translocation to the nucleus involved dissociation from myosin-9. In complex with PAD4, myosin-9 was citrullinated at both N-terminal and C-terminal sites in RA patients, but not in healthy controls. Citrullinated peptides corresponding to these sites were recognized by IgG autoantibodies in RA patients. We conclude that at least a portion of intracellular PAD4 in neutrophils interacts physically and catalytically with a myosin-9 containing macromolecular machinery involved in the cell migration and transport of organelles and membrane. (248 words).