Digitate shell morphologies have evolved repeatedly in planktonic foraminifera throughout the Cretaceous and Cenozoic. Digitate species are usually rare in fossil and modern assemblages but show increased abundance and diversity at times during the Cretaceous and middle Eocene. In this paper we discuss the morphology and stratigraphic distribution of digitate planktonic foraminifera and establish the isotopic depth ecology of fossil ones to draw parallels with modern counterparts. δ18O and δ13C values of six extinct and two modern digitate species, from six time slices (Cenomanian, Turonian, Eocene, Miocene, Pleistocene and Holocene) have similar isotopic depth ecologies, consistently registering the most negative δ13C and usually the most positive δ18O compared to coexisting species. These results indicate a similar deep, subthermocline (>150 m) habitat, characterized by lower temperatures, reduced oxygen, and enrichment of dissolved inorganic carbon. This is consistent with water-column plankton studies that provide insight into the depth preferences of the three modern digitate species; in over 70% of observations digitates occurred in nets below 150 m, and down to 2000 m. The correlation between digitate species and subsurface habitats across multiple epochs suggests that elongated chambers were advantageous for survival in a deep mesopelagic habitat, where food is usually scarce. Increased abundance and diversity of digitates in association with some early and mid-Cretaceous oceanic anoxic events, in middle Eocene regions of coastal and equatorial upwelling, and occasionally in some modern upwelling regions, suggests an additional link with episodes of enhanced ocean productivity associated with expansion of the oxygen minimum zone (OMZ). We suggest that the primary function of digitate chambers was as a feeding specialization that increased effective shell size and food gathering efficiency, for survival in a usually food-poor environment, close to the OMZ. Episodes of increased digitate abundance and diversity indicate expansion of the deep-water ecologic opportunity under conditions that were unfavorable to other planktonic species. Our results provide evidence of iterative evolution reflecting common functional constraints on planktonic foraminifera shell morphology within similar subsurface habitats. They also highlight the potential of digitate species to act as indicators of deep watermasses, especially where there was expansion of the OMZ.