Mitogen activated protein kinase (MAPK) signaling pathways execute essential functions in eukaryotic organisms by transducing extracellular stimuli into adaptive cellular responses. In the fission yeast model  Schizosaccharomyces pombe  the cell integrity pathway (CIP) and its core effector, MAPK Pmk1, play a key role during regulation of cell integrity, cytokinesis, and ionic homeostasis.  Schizosaccharomyces japonicus , another fission yeast species, shows remarkable differences with respect to  S. pombe , including a robust yeast to hyphae dimorphism in response to environmental changes. We show that the CIP MAPK module architecture and its upstream regulators, PKC orthologs Pck1 and Pck2, are conserved in both fission yeast species. However, some of  S. pombe 's CIP-related functions, such as cytokinetic control and response to glucose availability, are regulated differently in  S. japonicus.  Moreover, Pck1 and Pck2 antagonistically regulate  S. japonicus  hyphal differentiation through fine-tuning of Pmk1 activity. Chimeric MAPK-swapping experiments revealed that  S. japonicus  Pmk1 is fully functional in  S. pombe , whereas  S. pombe  Pmk1 shows a limited ability to execute CIP functions and promote  S. japonicus  mycelial development. Our findings also suggest that a modified N-lobe domain secondary structure within  S. japonicus  Pmk1 has a major influence on the CIP signaling features of this evolutionarily diverged fission yeast.