The extensive cytoplasmic regions of ER-phagy receptors suggest integration of ER remodelling with cytoplasmic changes. Here, we present a cytoplasmic interactome of prominent receptors. Within this, regulatory interactors of FAM134B/C are identified by targeted CRISPR/Cas9 screening. We identify PRKAR1A as a direct activator of FAM134B/C, binding through an amphipathic helix within the otherwise disordered C-terminal region of FAM134B. Super-resolution, FRAP and CLEM imaging demonstrate that irregular, liquid-like condensates of cAMP-bound PRKAR1A form ER contacts, promoting clustering of FAM134B with LC3B. Proximity proteomics reveal that cAMP induces FAM134B interaction with cytoplasmic RhoA, co-degradation within condensate-associated lysosomes, and reduction in peripheral actomyosin contractility. Physiologically, co-ordination of ER and cytoplasmic remodelling is required for canonical cAMP-regulated cell morphologic changes, including determination of the matrix invasion modality of cancer cells. In summary, bidirectional cross-talk between the ER and the cytoplasm is facilitated by FAM134B/C and cytoplasmic liquid condensates.