Far-red light photoacclimation exhibited by some cyanobacteria allows these organisms to use the far-red region of the solar spectrum (700–800 nm) for photosynthesis. Part of this process includes the replacement of six photosystem I (PSI) subunits with isoforms that confer the binding of chlorophyll (Chl)
f
molecules that absorb far-red light (FRL). However, the exact sites at which Chl
f
molecules are bound are still challenging to determine. To aid in the identification of Chl
f
-binding sites, we solved the cryo-EM structure of PSI from far-red light-acclimated cells of the cyanobacterium
Synechococcus
sp. PCC 7335. We identified six sites that bind Chl
f
with high specificity and three additional sites that are likely to bind Chl
f
at lower specificity. All of these binding sites are in the core-antenna regions of PSI, and Chl
f
was not observed among the electron transfer cofactors. This structural analysis also reveals both conserved and nonconserved Chl
f
-binding sites, the latter of which exemplify the diversity in FRL-PSI among species. We found that the FRL–PSI structure also contains a bound soluble ferredoxin, PetF1, at low occupancy, which suggests that ferredoxin binds less transiently than expected according to the canonical view of ferredoxin-binding to facilitate electron transfer. We suggest that this may result from structural changes in FRL-PSI that occur specifically during FRL photoacclimation.