We tested the hypothesis that cyanobacterial cells have sufficient acclimation potential to tolerate UVB when it is applied in a natural quantum ratio to growth photosynthetically active radiation (PAR). We grew Synechococcus under 50 (Low) or 300 (High) μmol PAR m⁻²·s⁻¹ and then exposed the cells to 0.125 (Low) or 0.75 (High) μmol UVB m⁻²·s⁻¹. The PAR:UVB quantum ratios were near natural for both the Low-PAR:Low-UVB and the High-PAR:High-UVB treatments, but UVB was in excess of typical aquatic PAR:UVB for Low-PAR:High-UVB treatments. The cellular light history determined the UVB responses of Synechococcus. High-PAR cells initially had fewer cpc transcripts encoding phycocyanin, lower phycocyanin content, and more psbAII/AIII transcripts encoding the D1:2 photosystem II (PSII) protein isoform. Higher PAR potentiated them to tolerate an appropriate UVB level without short-term inhibition of PSII or growth. Low-PAR cells rapidly altered psbAII/AIII and cpc gene expression and tolerated appropriate Low UVB. Low-PAR:High-UVB cells, in contrast, suffered short-term inhibition of PSII and growth. In all treatments UVB induced transient loss of cpc transcripts, possibly to free resources for psbAII/AIII expression, which is important for UVB resistance. The drop in cpc transcripts was not part of a general shock response because rbcL transcript pools were stable upon UVB exposure.