Osteoclasts, specialized bone resorbing cells of hematopoietic origin, become overactive in rheumatoid arthritis, leading to bone loss and joint destruction. Osteoclast progenitor cells (OCP) arise from myeloid precursors of monocyte/macrophage lineage and are normally present in the bone marrow and among circulatory monocytes. Under inflammatory conditions their subpopulations get attracted to inflamed sites by yet unknown mechanisms and chemotactic signals. Here, we investigated frequencies and chemokine receptor expression of OCP subpopulations in circulation and periarticular bone marrow (PBM) of C57BL/6 mice with collagen induced arthritis (CIA). We found both lymphoid-negative CD45+CD11b+CD115+ and lymphoid-negative CD45+CD11b-/loCD115+ subsets of OCPs to be increased in blood and PBM of affected joints in CIA. Chemokine receptors were increasingly expressed by both mentioned OCP subsets in CIA, with substantial expression of CCR2 and CX3CR1, and lower expression of CCR1, CCR3, CCR5, CCR9 and CXCR4. CCL2 serum levels, and gene expression for TNF-α, IL-1β, IL-6 and CCL2 in affected areas and spleen were significantly increased in CIA. PBM population of OCP increasingly migrated toward CCL2 chemotactic gradient, whereas down-regulation of CCR2 expression by siRNA significantly reduced the migration potential. Intravascular in vivo staining demonstrated increased recirculation of CD45+CD11b+ cells through PBM and hind paws in CIA, with the ability of tissue homing after adoptive transfer. These results suggest that highly induced OCP subpopulations in CIA migrate to inflamed joints due to chemotaxis and therefore blocking of chemokine signaling may reduce osteoclast activity in arthritis.