The transcription factor "Early Growth Response 4" (EGR4) has previously been identified as having a critical role in the proliferation of small cell lung cancer. Here, we have identified a novel, shortened splice variant of this transcription factor (EGR4-S) that is regulated by Heat Shock Factor-1 (HSF1). Our findings demonstrate that the shortened EGR4-S variant is upregulated in breast cell lines expressing high EGFR, HER2, and H-Rasv12, and that EGR4-S expression is inhibited in response to targeted cancer therapeutics acting on the HER pathway. However, sustained, high-dose therapy led to EGR4-S becoming less responsive. Protein and mRNA analyses of HER2+ human breast tumours indicated the novel EGR4-S splice variant to be preferentially expressed in tumour tissue and not detectable in patient-matched normal tissue. Knockdown of EGR4-S in the HER2-amplified breast cancer cell line SKBR3 reduced cell growth, suggesting that EGR4-S supports the growth of HER2+ tumour cells. In addition to targeted inhibitors of the HER2 pathway, EGR4-S expression was also found to be suppressed when molecular stress was elevated (with both chemical stressors or the overexpression of HSF1). Under conditions of increased molecular stress, reduced EGR4-S levels were associated with the observed lower cell growth rate but the augmentation of properties associated with higher metastatic potential. Taken together, our research suggests further investigation of EGR4-S is warranted in order to determine its potential as a biomarker for differentiating tumours from normal tissue at the molecular level, as well as its possible resistance to targeted therapies.