Manimaran (M. G. Ramachandran), is a doctor living in the country of Neidhal Naadu with his sidekick Azhaga (Nagesh). He helps cure the illness of one of the rebels against the dictator (Manohar) of Neidhal Naadu. The ruler's guards arrest the rebels, along with Manimaran for helping them. Manimaran and the rebels are sold as slaves by the ruler to the nearby island called Kanni Theevu (Tamil for Virgin Islands), ruled by Sengappan. Manimaran leads the slaves, and fights for their rights.
Poongodi (Jayalalithaa), the princess of Kanni Theevu and niece of Sengappan who is the guardian of the orphaned princess, falls in love with Manimaran at first sight. Simultaneously, her servant Thenmozhi (Madhavi Krishnan) falls for Azhagan, after initial arguments. Despite the differences between Poongodi and Manimaran, Poongodi tries to woo him on many occasions. She even offers freedom from slavery only to him, who rejects the offer demanding freedom for all of the slaves. Meanwhile, the island is attacked by pirates headed by a leader (M. N. Nambiar). As Sengappan's troops are out of the island on another assignment, Sengappan pleads with Manimaran and the other slaves to help him. Manimaran demands freedom slavery in return for fighting the pirates, only to be betrayed later.
The slaves make an escape plan of their own and successfully take over the pirate ship, with whom they fought earlier. Manimaran explains to the pirate captain/leader, about their plight and asks him to help them reach Neidhal Naadu. The captain, apparently agrees, while actually taking them to his pirate island and holds them captive. He coerces them to work for him as pirates or Manimaran will see all of his other men die before him. With no option in place, Manimaran agrees to work as a pirate to escape the situation. In one of his pirate hunts, he finds Sengappan and Poongodi. He brings Poongodi to the pirate island, and tries to hide her from the pirate leader. Nanjappan, the right hand of the pirate leader, finds out tells the leader about Poongodi. As per the policy of the island, any treasure pirated must be auctioned and so Poongodi is also auctioned. After a tight bidding, Manimaran bids the highest, buys her and keeps her with him.
After few dramatic events, Manimaran gets married to Poongodi and as per the pirate island's laws the pirate leader cannot attempt to separate a married couple. The pirate leader attempts to take Poongodi by force, gets defeated by Manimaran in a sword fight and reforms into a good man. He accompanies the slaves led by Manimaran, to achieve their goal of freeing Neidhal Naadu from the clutches of its cruel dictator. In the ensuing war, the dictator is defeated but tricks into arresting them instead. However, in his court the dictator begs Manimaran to take over the throne. Everyone else also supports the idea. However, Manimaran politely rejects the offer and further states that he wants to continue his noble work as a doctor, serving the people. He then takes leave from the royal court and walks away with his wife and his medical kit.M. G. Ramachandran as Manimaran, a doctor living in Neidhal NaaduJayalalithaa as Poongodi, the princess of Kanni TheevuM. N. Nambiar as the Pirate LeaderNagesh as Azhaga, Manimaran's sidekickR. S. Manohar as the Dictator of Neidhal NaaduMadhavi Krishnan as Thenmozhi, Azhaga's love interest
Aayirathil Oruvan was M. G. Ramachandran's first film with director B. R. Panthulu. It was also the first film which featured him alongside the-then newcomer Jayalalithaa, who was previously seen in her debut film Vennira Aadai. The duo subsequently starred together frequently in later films. Panthulu, who faced losses from his previous Karnan, compensated for it through this film. Aayirathil Oruvan is said to be inspired from the 1935 swashbuckling Errol Flynn starrer, Captain Blood, and also from Burt Lancaster's The Crimson Pirate, which itself was inspired by the 1926 film The Black Pirate. Shooting for some fight scenes and ship transportation scenes took place in Karwar.
The soundtrack of the film has been composed by Viswanathan–Ramamoorthy. It is the final film where the duo worked together, they subsequently composed for later films individually. The song "Atho Andha Paravai" remains one of the successful songs from the film. The song was featured in self-titled 2010 film of same name. The song was remixed by D. Imman with different vocals, tune and instrumentations in Madrasi (2006). The song "Naanamo" was remixed as "Roseberry" in Pallikoodam (2007). In Unnai Thedi (1999), Malavika's family will be seen watching "Naanamo". One of the songs has inspired a film's title "Unnai Naan Sandhithen". In Inidhu Inidhu Kaadhal Inidhu (2003), Vadivelu who is in female disguise imitates Jayalalitha's mannerisms and dances for "Aadamal Aadugiren'.
Aayirathil Oruvan was very well received by critics. Ramachandran's performance as a kind, noble, and brave leader later helped him build a massive reputation in his political career. On Ramachandran's centenary in January 2017, Nivedita Mishra of Hindustan Times included his performance in Aayirathil Oruvan in her list compiling "some of his most memorable performances".
Forty-nine years after the original theatrical release, the film was digitally enhanced for a planned re-release in January 2014. Apart from scope conversion from 35 mm to digital scope, the film also had a completely re-recorded background music played out by an assistant of M. S. Viswananthan. The digital conversion was done by Prasad EFX, Chennai, who had previously restored Karnan and Paasa Malar. Since the negatives were entirely damaged, the entire running length was converted. The film was distributed by Divya Films which had earlier released Karnan in digital format. The digitised version of Aayirathil Oruvan was released on 14 March 2014, earning ₹26.9 lakh (US$42,000) in the first weekend at Chennai; it eventually had a theatrical run of 190 days in Chennai.