Phosphorous in its inorganic form, orthophosphate (Pi), is found in every compartment of the plant cell and serves as a substrate, product or effector for a wide range of metabolic processes. Several Pi transporters exist in plants and these help regulate Pi homeostasis within different cellular compartments. The PHT4 family of organellar Pi transporters consists of six members in the model plant Arabidopsis thaliana, and five of these are localized to plastids. I used gene expression analyses and reverse genetics to demonstrate functional specialization for the PHT4 family members with a focus on PHT4;1 and PHT4;2. The PHT4;1 Pi transporter is localized to chloroplast thylakoid membranes and it is expressed in a circadian manner. Plants that lack a functional copy of the PHT4;1 gene have reduced rosette size and altered responses to photooxidative stress. The PHT4;2 transporter is localized to heterotrophic plastids in roots and other sink organs and pht4;2 mutants exhibit decreased starch accumulation, which is consistent with a defect in Pi export, and increased rosette size, which is caused by increased cell proliferation. These results confirm that PHT4;1 and PHT4;2 have specialized functions and that plastidic Pi homeostasis influences broad aspects of plant metabolism, including abiotic stress response and control of lateral organ growth.