Abstract Growing summer season and increased anthropogenic activities pose a continual challenge to resident species. Ectotherms like insects are especially vulnerable to rapid climatic changes. High-altitude tropical insect populations have been rarely examined for their responses to high-temperature. We exposed a tropical out-bred highland population of Drosophila melanogaster from the Himalayas to growing summer conditions in outdoor mesocosm units. Population response to thermal changes was tracked over ninety days at both phenotypic and genotypic level. Whole genomic resequencing data suggested a clear seasonal shift in allele frequencies. Interestingly, the general heat responsive genes were missing in the summer due to monsoon allele shift; an atypical response noted for high-altitude tropical populations. Instead, candidates involved in kinases and phosphorylation emerged as key players. Heat-knockdown time decreased over time indicating a limited ability to handle increasing temperature. Merging data from both allelic shifts and heat-knockdown time indicated a limited capacity for high-altitude insects in coping with climate warming.