ordered by the CIA to aid Naked Snake in Operation Snake Eater, in which The Boss, the Cobra Unit, and the threat of the Shagohod were to be eliminated, while also retrieving the Philosophers' Legacy for the American branch of the Philosophers. Returning to Rassvet, Ocelot intended to make contact with Snake, but the supposed KGB spy EVA reached him first, helping him evade Ocelot's unit. While Snake neutralized the Ocelot Unit, Ocelot himself captured EVA and held her at knife point, brandishing his new revolver at Snake. However, having apparently misspent his ammunition, due to SAA carrying fewer rounds than he was used to, Ocelot was roundly defeated. Ocelot fled the area, with Snake stopping EVA from gunning him down, allegedly because he was "still young," althoughhe had actually had taken a liking to him.

Maintaining his cover as a GRU operative, Ocelot decided to aid Snake covertly, and throughout Operation Snake Eater, the two developed a mutual rivalry and fought on several more occasions. Ocelot re-encountered Snake at the Bolshaya Past crevice, where they had a gun duel. However, it was interrupted with The Pain's hornets scouting ahead, forcing him to flee. Reaching the Ponizovje warehouse, Ocelot rendezvoused with Volgin and the Boss, where he he intimidated the uncooperative scientist Sokolov in a game of Russian roulette, almost killing him before The Boss intervened. Due to his audacious actions in confronting Snake at Bolshaya Past, Ocelot was scolded by the Boss and had his revolver dismantled in the process.

At the fortress of Groznyj Grad,