Chromium occurs naturally in aqueous environments by weathering and leaching of rocks and can also originate from industria anthropogenic sources. Here we investigate the different responses of phytoplankton to high levels of Cr exposure, which reveal contrasting strategies for metal uptake and homeostasis in different algal lineages. At high Cr(VI) concentrations, red lineages experience growth inhibition through reduced photosynthetic capability, while green lineages are completely unaffected. Moreover, Cr(VI) has a more significant impact on the metallomes of red lineage algae, in which metal/P ratios increased with increasing Cr(VI) concentration for many trace elements. Green algae have higher specificity transporters to prevent Cr(VI) from entering the cell, and more specific intracellular stores of Cr within the membrane fraction than the red algae, which accumulate more Cr mistakenly in the cytosol fraction via lower affinity transport mechanisms. Green algal approaches require greater nutrient investments in the more numerous transport proteins required and management of specific metals, a strategy better adapted to the resource‐rich coastal waters. By contrast, the red algae are nutrient‐efficient with fewer and less discriminate metal transporters, which can be fast and better adapted in the oligotrophic, oxygenated open ocean, which has prevailed since the deepening of the oxygen minimum zones at the start of the Mesozoic era.