The Hippo pathway was discovered to control tissue growth in Drosophila and includes the Hippo kinase (Hpo; MST1/2 in mammals), scaffold protein Salvador (Sav; SAV1 in mammals), and the Warts kinase (Wts; LATS1/2 in mammals). Hpo signalling inactivates the transcriptional co-activator Yorkie (Yki; YAP in mammals) by preventing its nuclear localisation. How the Hpo pathway responds to and integrates diverse molecular cues to modulate Yki/YAP activity, remains an outstanding question in the field. In epithelial cells, the Hpo kinase is organised at the apical domain by a cytoskeleton-dependent scaffold. This apical scaffold consists of Crumbs-Expanded (Crb-Ex) and Merlin-Kibra (Mer-Kib) complexes, which bind to and activate the Hpo kinase. We find that overexpressing Ex or Kib in the Drosophila follicular epithelium is sufficient to nucleate the formation of active, micron-sized Hpo complexes in the cytoplasm. The formation of supramolecular Hpo complexes can also be induced by starvation, mediated by inhibition of PI3K-Akt signalling. Hpo kinase complexes formed in vivo demonstrate characteristics of phase-separated biomolecular condensates, including liquid-like dynamics, concentration-dependence and sensitivity to known inducers (molecular crowding) and disruptors (1,6-hexanediol) of phase separation. Furthermore, purified Hpo-Sav complexes undergo phase separation in vitro. We find that the organisation of Hpo signalling components into condensates is conserved in mammalian cells, and concentration of active Hpo complexes at the apical domain of epithelial cells correlates with a YAP off state. Several Hpo pathway components are characterised by intrinsically disorder regions, and we predict these regions drive weak, multivalent interactions that underpin the condensate behaviour observed in this study. We propose that apical Hpo kinase activation occurs in phase separated ‘signalosomes’ induced by clustering of upstream pathway components.