Trinidadian guppies (Poecilia reticulata) are able to adapt to various environmental conditions and are even among the few species that can tolerate extensive pollution. In the Pitch Lake of Trinidad they live in highly toxic waters due to natural seepage of oil and bitumen. In this paper, we describe phenotypic divergence in several life-history traits between guppies from the Pitch Lake and from a nearby reference site with waters not polluted by bitumen/oil. We show that guppies from the Pitch Lake were (i) smaller and (ii) had a higher reproductive investment than those from the reference site. Furthermore, they (iii) produced more and smaller offspring. These results are congruent with a scenario of high mortality caused probably by a combination of water toxicity and higher predation than at the reference site. We therefore propose the Pitch Lake as an ideal system to study the effects of long-term (natural) water pollution on fishes, which might provide interesting insights into adaptation to extreme environments, and might further help to predict fish responses to anthropogenic pollution.