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Climate change is an imminent threat to livestock production. One adaptation strategy is selection for heat tolerance. While it is established that the <i>ATP1A1</i> gene and its product play an important role in the response to many stressors, there has been no attempt to characterize the sequence or to perform expression profiling of the gene in production animals. We undertook a field experiment to compare the expression profiles of <i>ATP1A1</i> in heat-tolerant Vechur and Kasaragod cattle (<i>Bos taurus indicus</i>) with the profile of a heat-susceptible crossbreed (<i>B. t. taurus</i> × <i>B. t. indicus</i>). The cattle were exposed to heat stress while on pasture in the hot summer season. The environmental stress was quantified using the temperature humidity index (THI), while the heat tolerance of each breed was assessed using a heat tolerance coefficient (HTC). The <i>ATP1A1</i> mRNA of Vechur cattle was amplified from cDNA and sequenced. The HTC varied significantly between the breeds and with time-of-day (<i>p</i> < 0.01). The breed–time-of-day interaction was also significant (<i>p</i> < 0.01). The relative expression of <i>ATP1A1</i> differed between heat-tolerant and heat-susceptible breeds (<i>p</i> = 0.02). The expression of <i>ATP1A1</i> at 08:00, 10:00 and 12:00, and the breed–time-of-day interaction, were not significant. The nucleotide sequence of Vechur <i>ATP1A1</i> showed 99% homology with the <i>B. t. taurus</i> sequence. The protein sequence showed 98% homology with <i>B. t. taurus</i> cattle and with <i>B. grunniens</i> (yak) and 97.7% homology with <i>Ovis aries</i> (sheep). A molecular clock analysis revealed evidence of divergent adaptive evolution of the <i>ATP1A1</i> gene favoring climate resilience in Vechur cattle. These findings further our knowledge of the relationship between the <i>ATP1A1</i> gene and heat tolerance in phenotypically incongruent animals. We propose that <i>ATP1A1</i> could be used in marker assisted selection (MAS) for heat tolerance.