Abstract Temporal thermal heterogeneity is expected to favour intermediate, generalist phenotypes that can maintain growth across a broad thermal range but have sub-optimal growth at any single temperature. Yet, thermal variation typically occurs in the presence of additional selection pressures which may interact to constrain adaptation to temperature. We propagated competing lytic viral parasites (bacteriophages, thermal specialist φ14–1 and thermal generalist φLUZ19) of Pseudomonas aeruginosa under fluctuating temperatures (37°C–42°C) in monoculture and in co-culture. Without competition, fluctuating temperatures resulted in intermediate thermal phenotypes in the phage φ14–1 and, in both phages, resulted in more variable evolutionary outcomes compared to static conditions. Selection from both fluctuating temperatures and competition accelerated thermal adaptation in the phage φ14–1. However, co-selection led to restricted thermal adaptation, lower genetic distance from ancestor, and fewer putative adaptive mutations in the phage φLUZ19. Our study highlights the potential for variable adaptive capacity in interacting communities amidst global climate change.