The planetary short-chain alkanes budget is impacted by methanogenic and alkanotrophic archaea in anaerobic environments. These anaerobes generate methane and degrade alkanes through alkyl-coenzyme M reductases (ACRs). Recent breakthroughs describe new alkanotrophs and their intriguing physiology in greater detail, but only sporadic studies exist on their alkane-degrading enzymes due to the absence of isolates and the challenge of preserving the natural intrinsic features of the protein. Here, we review differences in ACR traits and compare them to the extensively studied methane-generating counterpart. By describing the complexity of ACRs in their cofactors, architectures, post-translational modifications, and accessory proteins, we propose functional characteristics that may be shared among these enzymes and highlight the challenges of their recombinant expression. Gaining insights into the biochemical and structural traits of ACRs will unveil the molecular basis for short-chain alkane microbial transformation and new roads to their application, stimulating future directions in this continuously growing field.