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The photosynthetic amoeba, Paulinella provides a recent (ca. 120 Mya) example of primary plastid endosymbiosis. Given the extensive data demonstrating host lineage‐driven endosymbiont integration, we analysed nuclear genome and transcriptome data to investigate mechanisms that may have evolved in Paulinella micropora KR01 (hereinafter, KR01) to maintain photosynthetic function in the novel organelle, the chromatophore. The chromatophore is of α‐cyanobacterial provenance and has undergone massive gene loss due to Muller's ratchet, but still retains genes that encode the ancestral α‐carboxysome and the shell carbonic anhydrase, two critical components of the biophysical CO2 concentrating mechanism (CCM) in cyanobacteria. We identified KR01 nuclear genes potentially involved in the CCM that arose via duplication and divergence and are upregulated in response to high light and downregulated under elevated CO2. We speculate that these genes may comprise a novel CO2 delivery system (i.e., a biochemical CCM) to promote the turnover of the RuBisCO carboxylation reaction and counteract photorespiration. We posit that KR01 has an inefficient photorespiratory system that cannot fully recycle the C2 product of RuBisCO oxygenation back to the Calvin‐Benson cycle. Nonetheless, both these systems appear to be sufficient to allow Paulinella to persist in environments dominated by faster‐growing phototrophs. [ABSTRACT FROM AUTHOR]