WAVE3, an actin cytoskeleton remodeling protein, is highly expressed in advanced stages of breast cancer and influences tumor cell invasion. Loss of miR‐31 has been associated with cancer progression and metastasis. Here, we show that the activity of WAVE3 to promote cancer cell invasion is regulated by miR‐31. An inverse correlation was demonstrated between expression levels of WAVE3 and miR‐31 in invasive versus noninvasive breast cancer cell lines. miR‐31 directly targeted the 3'‐UTR of the WAVE3 mRNA and inhibited its expression in the invasive cancer cells, i.e., miR‐31‐mediated down‐regulation of WAVE3 resulted in a significant reduction in the invasive phenotype of cancer cells. This relationship was specific to the loss of WAVE3 expression because re‐expression of a miR‐31‐resistant form of WAVE3 reversed miR‐31‐mediated inhibition of cancer cell invasion. Furthermore, expression of miR‐31 correlates inversely with breast cancer progression in humans, where an increase in expression of miR‐31 target genes was observed as the tumors progressed to more aggressive forms. In conclusion, a novel mechanism for the regulation of WAVE3 expression in cancer cells has been identified, which controls the invasive properties of cancer cells. The study also identifies a critical role for WAVE3, downstream of miR‐31, in the invasion‐metastasis cascade.