Cancer cell plasticity, which is commonly referred to as epithelial to mesenchymal transition (EMT), plays a significant role in facilitating cancer cell invasion, tumor metastasis, and therapy resistance. Understanding and treating cancers that have progressed to metastatic, and therapy resistant states remains a crucial challenge. In a screen for novel regulators of EMT, we identified ZCCHC24, an uncharacterized CCHC-type zinc finger protein, as a potential modulator of breast cancer cell plasticity. ZCCHC24 is repressed by the epithelial-specific miR-200 family in epithelial cells, and it is highly induced in mesenchymal cells that lack miR-200. Unlike canonical EMT transcription factors, we identified ZCCHC24 as a cytoplasmic mesenchymal state specific RNA binding protein (RBP) that influences breast cancer cell plasticity through widespread post transcriptional changes in gene expression. Using CLIP-sequencing, we identified hundreds of RNA targets of ZCCHC24, but no specific binding motif was observed. However, ZCCHC24 bound near a consensus motif for the Pumilio RBP in many cases and physically interacted with Pumilio. Pumilio depletion impairs ZCCHC24-mediated functions, indicating a cooperative role for these RBPs. Functional studies revealed that ZCCHC24 knockout reduces mesenchymal features along with migratory and invasive capacity, whereas overexpression promotes these phenotypes. In vivo ZCCHC24 depletion significantly decreases breast cancer metastasis to multiple organs. We propose that ZCCHC24 is a novel regulator of cancer-associated EMT and gaining an understanding of how it operates may offer new treatment avenues for epithelial-derived cancers.