Triple-negative breast cancer (TNBC) is an aggressive subtype of breast cancer with limited treatment options. Distant metastasis is the leading cause of breast cancer deaths. Better understanding of metastasis regulation is needed for developing anti-metastasis treatment. One of the mechanisms by which cancer cells navigate the harsh metastasis process is epithelial-mesenchymal plasticity (EMP). Metastatic cancer cells often display hybrid E/M states, where the mesenchymal phenotypes facilitate their invasion and dissemination, and the epithelial phenotypes facilitate their colonization at the secondary organs. The EMP regulatory pathways offer potential treatment opportunities to suppress metastasis. However, most well-characterized EMP regulators are transcription factors, splicing factors, or micro-RNAs, which are difficult to target. Membrane proteins are very druggable and can be targeted for functional perturbation or as a non-functional target for antibody-drug conjugates or cell therapies. However, membrane regulators of EMP are less studied. Here we show that Eph Receptor A4 (EPHA4), a receptor tyrosine kinase that regulates cell repulsion during development, also regulates cell-cell adhesion, EMP, and metastasis in TNBC. Using bulk and single-cell RNA-seq, we found loss of EPHA4 can potentiate the expression of cell-cell adhesion genes and epithelial genes in both MDA-MB-231 and 4T1 TNBC tumors, thereby enabling a hybrid E/M transcriptional profile. Although loss of EPHA4 did not change spontaneous metastasis in 4T1, it increased the lung colonization burden in both models, consistent with the enhanced epithelial gene expression. We observed broad but model-dependent compensatory changes in the expression level of other Eph/Ephrin family genes, suggesting that targeting one member may not be sufficient to fully repress signaling by the Eph/Ephrin family. Together, our results revealed a previously unknown role of EPHA4 in regulating EMP and metastatic colonization in TNBC.