The worldwide increasing recourse to chemical dispersants to deal with oil spills in marine coastal ecosystems is a controversial issue. Yet, there exists no adequate methodology that can provide reliable predictions of how oil and dispersant-treated oil can affect relevant organism or population-level performance. The primary objective of the present study was to examine and compare the effects of exposure to untreated oil (weathered Arabian light crude oil), chemically dispersed oil (Finasol, TOTAL-Fluides) or dispersant alone, upon the ability of fish for environmental adaptation. To reach that goal, we implemented high-throughput, non-lethal challenge tests to estimate individual hypoxia and heat tolerance as surrogate measures of their capacity to face natural contingencies. Experimental populations were then transferred into semi-natural tidal ponds and correlates of individuals' fitness (growth and survival) were monitored over a period of 6 months. In accordance with our stated objectives, the contamination conditions tested corresponded to those observed under an oil slick drifting in shallow waters. Our results revealed that the response of control fish to both challenges was variable among individuals and temporally stable (repeatable) over a 2-month period. Exposure to chemical dispersant did not affect the repeatability of fish performance. However, exposure to oil or to a mixture of oil plus dispersant affected the repeatability of individuals' responses to the experimental challenge tests. At population level, no difference between contamination treatments was observed in the distribution of individual responses to the hypoxia and temperature challenge tests. Moreover, no correlation between hypoxia tolerance and heat tolerance was noticed. During the field experiment, hypoxia tolerance and heat tolerance were found to be determinants of survivorship. Moreover, experimental groups exposed to oil or to dispersant-treated oil displayed significantly lower survival than control or dispersant-exposed groups. Finally, from the four experimental populations tested, the one exposed to chemically dispersed oil presented the lowest growth rate.