Destroyer's Rubies received widespread acclaim from contemporary music critics. At Metacritic, which assigns a normalized rating out of 100 to reviews from mainstream critics, the album received an average score of 88, based on 30 reviews, which indicates "universal acclaim". Matt LeMay of Pitchfork gave the album a very favorable review, stating: "The album is structurally complex, thematically dense, and labyrinthine in its self-referentiality. Dan Bejar's vocals are, like many of his indie contemporaries, yelpy and dramatic, and many of his lyrics seem preordained to serve as mp3 blog headers. In other words, the qualities that once made Destroyer albums so "difficult" make Destroyer's Rubies a perfect record for this critical moment."
Pitchfork placed Destroyer's Rubies at number 158 on their list of the top 200 albums of the 2000s.