Irwin Allen was born in New York City, the son of poor Jewish immigrants from Russia. He majored in journalism and advertising at Columbia University after attending City College of New York for a year. He left college because of financial difficulties caused by the Great Depression. He moved to Hollywood in 1938, where he edited Key Magazine followed by an 11-year stint producing his own program at radio station KLAC. The success of the radio show led to him being offered his own gossip column, Hollywood Merry-Go-Round, which was syndicated to 73 newspapers. He produced his first TV program, a Celebrity panel show also called Hollywood Merry-Go-Round with announcer Steve Allen, before moving into film production.

Allen became involved in film production at a time when power was beginning to shift from studios to talent agencies. He put together packages consisting of Directors, actors and script, and sold them to film studios. After producing Where Danger Lives (1950) and Double Dynamite (1951) for RKO, Allen made his directorial debut with the documentary The Sea Around Us (1953).

The Sea Around Us was based on Rachel Carson's best-selling book of the same name. It was made with largely stock footage and won the 1952 Academy Award for Best Documentary Feature. Carson was so disappointed with Allen's final version of the script that she never again sold film rights to her work. The film includes gory images of whales being killed that are more shocking to modern audiences than they were at the time.

Allen returned to producing with the 3-D film Dangerous Mission (1954) before directing a semi-documentary about the evolution of life, The Animal World (1956). Again he made heavy use of stock footage, but he also included a nine-minute stop-motion dinosaur sequence by Ray Harryhausen. Before release, he toned down the gore from both the live action and the animation.

His next film, The Story of Mankind (1957), is a very loose adaptation of the Hendrik Willem van Loon book of the same name. It featured many well-known actors, some nearing the end of their careers, including the Marx Brothers, Ronald Colman, Hedy Lamarr, Vincent Price, and a young Dennis Hopper. The actors were each paid $2,500 for a single day's work with Allen relying on stock footage for the rest of the film.

Allen co-wrote and produced The Big Circus (1959) for Allied Artists Pictures before co-writing, producing and directing his next three films for 20th Century Fox: The Lost World (1960), Voyage to the Bottom of the Sea (1961), and Five Weeks in a Balloon (1962). The Lost World was the first of many films and TV shows Allen would make for 20th Century-Fox. Willis O'Brien, who worked on the pioneering special effects of the original Lost World (1925) and King Kong (1933) films, was disappointed when Allen opted to save time by using live alligators and lizards instead of stop-motion animation for the film's dinosaurs. Voyage to the Bottom of the Sea was a scientifically dubious, Jules Verne-style adventure to save the world from a burning Van Allen belt. It was the basis for his later television series of the same name. The family film Five Weeks in a Balloon was a loose adaptation of the Verne novel.

Allen also produced several TV movies, such as City Beneath the Sea, which recycled many props and Models from Voyage, Lost in Space, and Man From The 25th Century. Both were intended as pilots for new TV series projects, but his small-screen success from the 1960s largely eluded him in the 1970s. Lost in Space's Bill Mumy said of Allen that, while he was very good at writing television pilots that sold, his unwillingness to spend money hurt his shows' quality once on the air. A Monster costume that appeared on one of his shows, for Example, would appear on another a few weeks later with new paint. Writer Jon Abbott described Allen as paradoxical. "Here was a man who, when told the cost of a spaceship for a Lost in Space alien, snapped, 'Let him walk!' ... and then let the show be canceled rather than take a cut in the budget".

Voyage to the Bottom of the Sea (1964–68, ABC TV) established both Allen's and 20th Century Fox's reputation as television producers. The financial viability of the series was enormously helped by the re-use of many of the sets from the film; the cost of the Seaview submarine sets alone exceeded the budget of a typical pilot show of the era. The series also benefited from Allen's now notorious use of stock Fox film footage, particularly from Hell and High Water, The Enemy Below and Allen's The Lost World.

Allen originally intended Lost in Space (1965–68, CBS TV) to be a family show, a science-fiction version of The Swiss Family Robinson. It quickly developed into a children's show with episodes concentrating on the young Will Robinson, the robot and especially the comic villain Dr. Smith. The show popularized several science-fiction elements that have since become widespread, such as the comic robot (e.g. Silent Running, Star Wars) or android (Logan's Run, Star Trek: The Next Generation), the heroic kid (Voyagers!, Wesley Crusher), and the wacky lovable alien (Albert in Alien Nation, Vir in Babylon 5).

The Time Tunnel (1966–67, ABC TV), with each episode set in a different historical time period, was an ideal vehicle for Allen's talent for smoothly mixing live action with footage from Fox films set in the periods shown in the episode. The series was Allen's most visually impressive, comparing well with the contemporaneous Star Trek once the crew left the Enterprise. A change in network management led to the show being cancelled after just one season.

Land of the Giants (1968–70, ABC TV) was the most expensive show of its day at roughly $250,000 per episode. As another castaway themed show, Allen incorporated some of the successful elements from Lost in Space, although this time he did not allow the treacherous character to dominate the series.

In the late 1970s and mid-1980s, Allen sporadically returned to TV with miniseries efforts such as The Return of Captain Nemo/The Amazing Captain Nemo (1978) and a star-studded version of Alice in Wonderland (1985), as well as television series The Swiss Family Robinson (1975–76) and Code Red (1981–82). He planned to make a star-studded musical of Pinocchio, but his declining health forced his retirement in 1986. Allen was awarded a Worst Career Achievement Golden Raspberry Award in 1985.

After The Towering Inferno, he left 20th Century Fox when a change in management cancelled the remaining three planned disaster films. He was offered work at Warner Bros. by Jon Calley, who built an office building for Allen. Allen continued to work there for the remainder of his career. He produced several made-for-TV disaster movies: Flood! (1976), Fire! (1977), Hanging by a Thread (1979), The Night the Bridge Fell Down (1979), and Cave-In! (1979). For theatrical release, he produced and directed The Swarm (1978) and Beyond the Poseidon Adventure (1979), and produced When Time Ran Out (1980). Despite this success, the rise of new filmmakers like George Lucas caught him off guard. The success of Star Wars reportedly bewildered him; he could not understand how a film with apparently no stars or love story could enrapture audiences so fervently.

Episode 57 of the Disney TV series Duck Tales screened December 8, 1987, titled "The Uncrashable Hindentanic" features a character called "Irwin Mallard" who films the destruction of Scrooge McDuck's airship called the Hindentanic in the disaster movie style of Irwin Allen.

Allen died from a heart attack on November 2, 1991.

In 1994, while Senior VP of Foxstar, Burns founded Van Ness Films, a non-fiction and documentary production unit. That same year, he met Jon Jashni, a Fox film executive who shared Burns' interest in Allen's works.

Allen's career in film and TV was the subject of a 1995 documentary, The Fantasy Worlds of Irwin Allen, produced and directed by Kevin Burns, co-founder of Foxstar Productions, originally set up as the production unit responsible for creating a series of "Alien Nation" movies for television. Numerous cast members and associates from various Irwin Allen projects appeared in the film, lending recollections of their time working with him.

It also was used as a vehicle to promote the 1998 Lost in Space movie version of the original television series, starring william Hurt, Matt LeBlanc, Gary Oldman, Lacey Chabert, Mimi Rogers and Heather Graham.

Burns and Jashni later formed Synthesis Entertainment and began developing and producing remakes of, and sequels to, several Allen properties, including a 2002 Fox Television pilot for an updated version of The Time Tunnel, which did not sell, and remakes of films including Poseidon (2006) and Voyage to the Bottom of the Sea. The 2002 TV pilot was included as a bonus feature on Volume 2 of Fox's 2006 DVD release of the 30-episode Time Tunnel (1966–67) TV series.

In the film Ocean's 13 (2007) Linus Caldwell (played by Matt Damon) announces aloud to the comatose Reuben Tishkoff that Rusty Ryan is doing an 'Irwin Allen' which is a reference to the fake earthquake they stage later in the story.

On January 3, 2008, BBC Four showed a night of Allen's work which included the 1995 documentary The Fantasy Worlds of Irwin Allen along with episodes of Lost in Space, Land of the Giants and Voyage to the Bottom of the Sea.