Transgenerational inheritance from both parental lines can occur by genetic and epigenetic inheritance. Maternal effects substantially influence offspring survival and fitness. However, investigation of the paternal contribution to offspring success has been somewhat neglected. Adult zebrafish were separated into female and male groups exposed for 21-days to either a control diet or to a diet containing water accommodated fractions of crude oil. Four F1 offspring groups were obtained: 1) control (non-exposed parents), 2) paternally-exposed, 3) maternally-exposed, and 4) dual parent-exposed larvae. To determine the maternal and paternal influence on their offspring, we evaluated responses from molecular to whole organismal levels in both generations. Growth rate, hypoxia resistance, and heart rate did not differ among parental groups. However, global DNA-methylation in heart tissue was decreased in oil-exposed fish compared with control parents. This decrease was accompanied by an up-regulation of glycine N-methyltransferase. Unexpectedly, maternal, paternal, and dual exposure all enhanced F1 survival of offspring raised in oiled conditions. Regardless of parental exposure, however, F1 exposed to oil exhibited bradycardia. Compared with offspring from control parents, global DNA-methylation was decreased in the three offspring groups derived from oil-exposed parents. However, no difference between groups was observed in gene regulation involved in methylation transfer, suggesting that the changes observed in the F1 populations may have been inherited from both parental lines. Phenotypic responses during exposure to persistent environmental stressors in F1 offspring appear to be influenced by maternal and paternal exposure, potentially benefitting offspring populations to survive in challenging environments.