Ocean acidification may impact the fitness of marine fish, however, studies reporting neutral to moderate effects have mostly performed short-term exposures to elevated CO2, whereas longer-term studies across life stages are still scarce. We performed a CO2 exposure experiment, in which a large number (n > 2200) of Atlantic silverside Menidia menidia offspring from wild spawners were reared for 135 days through their embryonic, larval, and juvenile stages under control (500 μatm) and high CO2 conditions (2300 μatm). Although survival was high across treatments, subtle but significant differences in length, weight, condition factor and fatty acid (FA) composition were observed. On average, fish from the acidified treatment were 4% shorter and weighed 6% less, but expressed a higher condition factor than control juveniles. In addition, the metrics of length and weight distributions differed significantly, with juveniles from the high CO2 treatment occupying more extreme size classes and the length distribution shifting to a positive kurtosis. Six of twenty-seven FAs differed significantly between treatments. Our results suggest that high CO2 conditions alter long-term growth in M. menidia, particularly in the absence of excess food. It remains to be shown whether and how these differences will impact fish populations in the wild facing size-selective predation and seasonally varying prey abundance.