<p>Diversification between littoral and pelagic habitats is widespread in the fishes adaptively radiating in lakes, suggesting that where it occurs offspring spawned in a non-ancestral habitat may face few negative effects. We used littoral and pelagic ecotypes of pumpkinseed sunfish (<i>Lepomis gibbosus</i>) to investigate performance over the natal summer of age-0 juveniles spawned either in the ancestral littoral habitat of a Canadian shield lake or in two other habitat types: exposed rocky littoral shorelines and submerged rocky shoals offshore in the pelagic habitat. We compared zooplankton availability and use through stable isotope analysis of juvenile tissue and subsequent effects on late natal summer size and condition among habitats. Zooplankton prey were three times more abundant at pelagic than at littoral and shoreline sites and stable isotope analysis revealed that the fraction of plankton-derived tissue was consistently higher in age-0 juvenile fish from pelagic sites. By summer’s end, age-0 pelagic juveniles were 15% longer and 35% heavier than littoral and shoreline juveniles, indicating that accessible planktonic resources provided significant growth benefits to juveniles in the pelagic but not inshore habitats. By addressing a key uncertainty about the effects of non-ancestral natal conditions on age-0 performance, our study reveals a previously unrecognized juvenile benefit of habitat diversification by pumpkinseed sunfish in a postglacial lake. Since larger juvenile size contributes to first year survival these benefits could enhance local recruitment to a pelagic subpopulation that favours ecological and phenotypic diversification of pumpkinseed ecotypes through interacting developmental and evolutionary mechanisms.</p>