The width of a population's resource-use niche is determined by individual diet breadth (“within-individual component”) and the degree of niche partitioning between individuals (“between-individual component”). The balance between these two factors affects ecological stability and evolutionary trajectories, and may shift as ecological opportunity permits broader population niches. Lakes in California’s Sierra Nevada Mountains vary in resource diversity for introduced brook trout (Salvelinus fontinalis) due to elevation, lake morphometry, and watershed features. We compared the relative contributions of within- and between-individual niche components to two measures of the dietary niches of thirteen populations of brook trout: prey taxonomic composition and prey size distribution. For both taxonomic and size diversity of fish diets, population niche width was positively related to both the within- and between-individual components. For taxonomic diversity, the two components increased in parallel, while for size diversity, the between-individual component became more important relative to the within-individual component in populations with the greatest niche widths. Our results support the Niche Variation Hypothesis that populations with broader niches are more heterogeneous among individuals and show that individual niche width and individual specialization can operate in parallel to expand the population niche.