1. The assumption that the primary limitations on reproductive success differ between the sexes is inherent in traditional sexual selection theory. Although the energy that can be allocated to reproduction is assumed to be the main limitation to females, the ability to attract and defend oestrous females is assumed to be the primary limitation to males. 2. Estimates of the energetic costs of reproduction in male mammals are, however, limited and have largely been obtained from sexually dimorphic species exhibiting female defence mating systems. These studies often reveal that the energetic cost of male reproduction is similar to or even exceeds that of females, and therefore challenge long-held assumptions of inter-sexual reproductive limitations, but their generality is little known. 3. We coupled measurements of energy expenditure with detailed behavioural observations of reproductive male North American red squirrels (Tamiasciurus hudsonicus). This species displays minimal sexual dimorphism and exhibits a scramble competition mating system, under which sexual selection favours enhanced mate searching effort by males. 4. We conducted the study over 2 years characterized by a substantial variation in upcoming natural food availability and across two study populations that experienced either natural food abundance or an ad libitum food-supplementation to investigate the influence of resource availability on male reproductive energy expenditure. 5. Under natural conditions, mean energy expenditure of males across the 2 years was high, approximating that of females during lactation. Furthermore, in the anticipation of high upcoming natural food availability and resultant offspring survival, expenditure approximately doubled (from 290 +/- 7 to 579 +/- 73 kJ day(-1)). When current food availability (and consequently the density of receptive females) was experimentally elevated, males displayed the highest levels of energy expenditure we recorded (873 +/- 98 kJ day(-1)). 6. Our results provide compelling evidence that the energy available for reproductive allocation places a strong limitation on reproduction in male North American red squirrels and contribute to previous work suggesting that high and limiting energetic costs of male reproduction may be a general feature of mammalian reproduction.