The phrase Rule 34 was coined from an August 13, 2003, webcomic captioned, "Rule #34 There is porn of it. No exceptions." The comic was drawn by TangoStari (Peter Morley-Souter) to depict his shock at seeing Calvin and Hobbes parody porn. Although the comic faded into obscurity, the caption instantly became popular on the Internet. Since then, the phrase has been adapted into different syntactic versions and has even been used as a verb. A list of "rules of the Internet", created on the website 4chan, includes Rule 34 within a list of similar tongue-in-cheek maxims, such as Rule 63.

In 2008, users on 4chan posted numerous sexually explicit parodies and cartoons illustrating Rule 34; in 4chan slang, pornography may be referred to as "rule 34" or "pr0nz". The Dictionary of Modern Proverbs claims that Rule 34 "began appearing on Internet postings in 2008".

As Rule 34 continued spreading throughout the Internet, some traditional media began reporting on it. A 2009 Daily Telegraph article listed Rule 34 as the third of the "Top 10" Internet rules and laws. A 2013 CNN story said Rule 34 was "likely the most famous" Internet rule that has become part of mainstream culture. On November 14, 2018, a Twitch streamer nicknamed "Drypiss" celebrated his 18th birthday by posting a video to Twitter in which he looked up Rule 34 pictures; afterwards, the video and its responses were covered by The Daily Dot.

Fan fiction has parodied events such as the 2016 United States presidential election, the 2021 Suez Canal obstruction, and Brexit.