The society is essentially a debating club. Meetings are held once a week, traditionally on Saturday evenings, during which one member gives a prepared talk on a topic, which is later thrown open for discussion; during the meetings, members used to eat sardines on toast, called "whales," though it's not known whether they still do. There are no constraints regarding which topic may be raised and how it is approached: members may raise any idea they can mount an argument for, no matter how controversial or politically incorrect.

The Apostles retain a leather diary of their membership stretching back to its founder, which includes handwritten notes about the topics each member has spoken on. The diary is retained by the secretary of the society. The members referred to as the "Apostles" are the active, usually undergraduate members; former members are called "angels". Undergraduates usually agree to become angels after graduating or being awarded a fellowship; they then look out for new members among the undergraduate population. Every few years, amid great secrecy, all the angels are invited to an Apostles' dinner at a Cambridge college.

Undergraduates being considered for membership are called "embryos" and are invited to "embryo parties," where members judge whether the student should be invited to join. The "embryos" attend these parties without knowing they are being considered for membership. Becoming an Apostle involves taking an oath of secrecy and listening to the reading of a curse, originally written by Apostle Fenton Hort, the theologian, in or around 1851.
There have been very few women members. The first woman to join, an American Ph.D student in social anthropology, became a member in 1985, 165 years after the society was founded.

Critics say the society's secretive nature, combined with the small number of women members, and the significant percentage of angels who have acquired fellowships at Cambridge, and positions in the media, government and the church, places the Apostles at odds with the meritocratic ideals the university espouses. Former members have spoken of the life-long bond they feel toward one another. Henry Sidgwick, the philosopher, wrote of the Apostles in his memoirs that "the tie of attachment to this society is much the strongest corporate bond which I have known in my life."

The Apostles came to public attention again following the exposure of the Cambridge spy ring in 1951. At least four men with access to the top levels of government in Britain — two of them former Apostles — were found to have passed information to the KGB. The four known agents were Guy Burgess, an MI6 officer and secretary to the deputy foreign minister; Anthony Blunt, MI5 officer, director of the Courtauld Institute, and art adviser to the Queen; Donald MacLean, foreign office secretary; and Kim Philby, MI6 officer and journalist.

Although only four men were identified, there were rumors of a fifth man, a senior British intelligence officer, who was never found. Many stories linked this rumor to Victor Rothschild, another Apostle, who had supplied an apartment in London for some of the Cambridge spies to meet in, though there is no evidence that he knew about their spying activities. In 1963, American writer Michael Straight, also an Apostle, and later publisher of his family's The New Republic magazine, admitted to spying.

Of the four named spies, Guy Burgess and Anthony Blunt, both homosexual, had been members of the Apostles at a time when homosexuality seemed to be an attribute of many of the undergraduates chosen for membership, and stories persisted that the membership was mainly homosexual and Marxist. Blunt, a communist, was the first to be recruited by the KGB, during a visit to Russia in 1933. When he returned to Britain, he recruited other Cambridge students, including Straight. * As the Queen's art advisor, Blunt was knighted in 1956, but was stripped of his knighthood in 1979 after Prime Minister Margaret Thatcher publicly named him as a spy.