Phycocyanin (PC) is a soluble phycobiliprotein found within the light-harvesting phycobilisome complex of cyanobacteria and red algae, and is considered a high-value product due to its brilliant blue colour and fluorescent properties. However, commercially available PC has a relatively low temperature stability. Thermophilic species produce more thermostable variants of PC, but are challenging and energetically expensive to cultivate. Here, we show that the PC operon from the thermophilic cyanobacterium
Thermosynechococcus elongatus
BP-1 (
cpcBACD
) is functional in the mesophile
Synechocystis
sp. PCC 6803. Expression of
cpcBACD
in an ‘Olive’ mutant strain of
Synechocystis
lacking endogenous PC resulted in high yields of thermostable PC (112 ± 1 mg g
−1
DW) comparable to that of endogenous PC in wild-type cells. Heterologous PC also improved the growth of the Olive mutant, which was further supported by evidence of a functional interaction with the endogenous allophycocyanin core of the phycobilisome complex. The thermostability properties of the heterologous PC were comparable to those of PC from
T. elongatus
, and could be purified from the Olive mutant using a low-cost heat treatment method. Finally, we developed a scalable model to calculate the energetic benefits of producing PC from
T. elongatus
in
Synechocystis
cultures. Our model showed that the higher yields and lower cultivation temperatures of
Synechocystis
resulted in a 3.5-fold increase in energy efficiency compared to
T. elongatus
, indicating that producing thermostable PC in non-native hosts is a cost-effective strategy for scaling to commercial production.