To overcome physical boundaries imposed by the tumour microenvironment, many invasive cancer cells form specialized protein complexes called invadopodia which actively degrade the surrounding matrix. β-adrenergic receptor (βAR) signalling has been shown to affect tumour cell invasion, however, the cellular basis by which this occurs is still not well understood. To address this, we investigated effects of βAR activation on the formation of invadopodia in breast cancer cells. βAR signaling increased both the percentage of invadopodia positive cells and number of invadopodia per cell in MDA-MB-231 cells. Investigation using selective ligands demonstrated β2AR signaling – but not β1AR - is required for increased invadopodia. Ectopic expression of β2AR induced invadopodia formation in MCF7 cells, which endogenously express β1AR, but not β2AR and otherwise do not form invadopodia. Consistent with a role for invadopodia in tumor cell invasion, β2AR activation enhanced 3D migration of breast cancer cells from primary tumour explants. Pre-treatment with the Src inhibitor PP2 blocked both invadopodia formation and 3D migration following β2AR activation, showing that β2AR invadopodia formation is dependent on Src. Our results identify β2AR as a novel molecular regulator of invadopodia formation and highlight a mechanism for the effects of stress responsive signaling on progression of cancer metastasis.