Rohmer's career began to gain momentum with a cycle of films that he titled Six Moral Tales. Each tale follows the same story, inspired by F. W. Murnau's Sunrise (1927): a man, married or otherwise committed to a woman, is tempted by a second woman but eventually returns to the first woman.

Rohmer first worked as a Teacher in Clermont-Ferrand. In the mid-1940s he quit his teaching job and moved to Paris, where he worked as a freelance Journalist. In 1946 he published a novel, Elisabeth (AKA Les Vacances) under the pen-name Gilbert Cordier. In about 1949, while living in Paris, Rohmer first began to attend screenings at Henri Langlois's Cinémathèque Française, where he first met and befriended Jean-Luc Godard, François Truffaut, Claude Chabrol, Jacques Rivette and other members of the French New Wave. Rohmer had never been very interested in film and always preferred literature but soon became an intense lover of films and switched from journalism to film criticism. He wrote film reviews for such publications as Révue du Cinéma, Arts, Temps Modernes and La Parisienne.

In 1950 Rohmer made his first 16mm short film, Journal d'un scélérat. The film starred Writer Paul Gégauff and was made with a borrowed camera. By 1951 Rohmer had a bigger budget provided by friends and shot the short film Présentation ou Charlotte et son steak. The 12-minute film was co-written by and starred Jean-Luc Godard. The film was not completed until 1961. In 1952 Rohmer began collaborating with Pierre Guilbaud on a one-hour short feature, Les Petites Filles modèles, but the film was never finished. In 1954 Rohmer made and acted in Bérénice, a 15-minute short based on a story by Edgar Allan Poe. In 1956 Rohmer directed, wrote, edited and starred in La Sonate à Kreutzer, a 50-minute film produced by Godard. In 1958 Rohmer made Véronique et son cancre, a 20 minute-short produced by Chabrol.

Rohmer's best-known article was "Le Celluloid et le marbre" ("Celluloid and Marble") in 1955, which examines the relationship between film and other arts. In the article, Rohmer states that in an age of cultural self-consciousness, film is "the last refuge of poetry" and the only contemporary art form from which metaphor could still spring naturally and spontaneously.

In 1957, Rohmer married Thérèse Barbet. The couple had two sons. Rohmer was a devout Catholic and "ecological zealot". For years Rohmer had no telephone and refused to even get into cars, which he called "immoral pollutors." For many years he was known to jog two miles to his office every morning. He was well known for his need for personal privacy and sometimes wore disguises, such as wearing a false moustache at the New York premiere of one of his films. Rohmer's mother died without ever knowing that her son Maurice was in fact a famous film Director named Éric Rohmer. He stated that his favorite film Director was Jean Renoir.

Chabrol's company AJYM produced Rohmer's feature directorial debut, The Sign of Leo (Le Signe du lion) in 1959. In the film an American Composer spends the month of August waiting for his inheritance while all his friends are on vacation and gradually becomes impoverished. It included music by Louis Sagver. The Sign of Leo was later recut and rescored by distributors when Chabrol was forced to sell his production company, and Rohmer disowned the recut version. In 1962 Rohmer and Barbet Schroeder co-founded the production company Les Films du Losange (they were later joined by Pierre Coltrell in the late 1960s). Les Films du Losange produced all of Rohmer's work (except his last three features produced by La Compagnie Eric Rohmer).

In 1963 Les Films du Losange produced the New Wave omnibus film Six in Paris, in which Rohmer's short "Place de l'Etoile" was the centerpiece. After being driven out of his Editor position at Cahiers du Cinema, Rohmer began making short documentaries for French television. Between 1964 and 1966 Rohmer made 14 shorts for television through the Office de Radiodiffusion Télévision Française (ORTF) and Télévision Scolaire. These films included episodes of Filmmakers of Our Time on Louis Lumiere and Carl Theodor Dreyer, educational films on Blaise Pascal and Stéphane Mallarmé, and documentaries on the Percival legend, the industrial revolution and female students in Paris. Rohmer later said that television taught him how to make "readable images". He later stated "When you show a film on TV, the framing goes to pieces, straight lines are warped...the way people stand and walk and move, the whole physical dimension...all this is lost. Personally I don't feel that TV is an intimate medium." In 1964 Rohmer made the 13-minute short film Nadja à Paris with Cinematographer Nestor Almendros.

Rohmer typically populates his movies with people in their twenties and the settings are often on pleasant beaches and popular resorts, notably in La Collectionneuse (1967), Pauline at the Beach (1983), The Green Ray (1986) and A Summer's Tale (1996). These films are immersed in an environment of bright sunlight, blue skies, green grass, sandy beaches, and clear waters. He explained that "people sometimes ask me why most of the main characters in my films are young. I don't feel at ease with older people...I can't get people older than forty to talk convincingly."

The fourth "Moral Tale" was My Night at Maud's in 1969. The film was made with funds raised by François Truffaut, who liked the script, and was initially intended to be the third "Moral Tale". But because the film takes place on Christmas Eve, Rohmer wanted to shoot the film on and around Christmas Eve. Actor Jean-Louis Trintignant was not available so filming was delayed for an entire year. The film centers on Pascal's Wager and stars Trintignant, Françoise Fabian, Marie-Christine Barrault and Antoine Vitez. My Night at Maud's was Rohmer's first successful film both commercially and critically. It was screened and highly praised at the 1969 Cannes Film Festival and later won the Prix Max Ophüls in France. It was released in the US and praised by critics there as well. It eventually received Oscar nominations for Best Original Screenplay and Best Foreign Film. James Monaco said that "Here, for the first time the focus is clearly set on the ethical and existential question of choice. If it isn't clear within Maud who actually is making the wager and whether or not they win or lose, that only enlarges the idea of "le pari" ("the bet") into the encompassing metaphor that Rohmer wants for the entire series."

Beginning in the late 1970s during the production of Perceval le Gallois Rohmer began to reduce the number of crew members on his films. He first dispensed of the Script supervisor, then (controversially) cut out the assistant Director, then all other assistants and technical managers until, by the time he shot The Green Ray in 1986, his crew consisted only of a camera operator and a sound Engineer. Rohmer stated that "I even wonder if I could work in the usual conditions of filmmaking."

The sixth and final "Moral Tale" was Love in the Afternoon (released as Chloe in the Afternoon in the US) in 1972. Film critic Molly Haskell criticized the film for betraying the rest of the series by making a moral judgment on the main character and approving of his decision in the film.

His style was famously criticised by Gene Hackman's character in the 1975 film Night Moves who describes viewing Rohmer's films as "kind of like watching paint dry".

Following the Moral Tales Rohmer wanted to make a less personal film and adapted a novella by Heinrich von Kleist, La Marquise d'O... in 1976. It was one of Rohmer's most critically acclaimed films, with many critics ranking it with My Night at Maud's and Claire's Knee. Rohmer stated that "It wasn't simply the action I was drawn to, but the text itself. I didn't want to translate it into images, or make a filmed equivalent. I wanted to use the text as if Kleist himself had put it directly on the screen, as if he were making a movie ... Kleist didn't copy me and I didn't copy him, but obviously there was an affinity."

In 1978 Rohmer made the Holy Grail legend film Perceval le Gallois, based on a 12th-century manuscript by Chrétien de Troyes. The film received mostly poor critical reviews. Tom Milne said that the film was "almost universally greeted as a disappointment, at best a whimsical exercise in the faux-naif in its attempt to capture the poetic simplicity of medieval faith, at worse an anticlimatic blunder" and that it was "rather like watching the animation of a medieval manuscript, with the text gravely read aloud while the images — cramped and crowded, coloured with jewelled brilliance, delighting the eye with bizarre perspectives — magnificently play the role traditionally assigned to marginal illuminations." In 1980 Rohmer made a film for television of his stage production of Kleist's play Catherine de Heilbronn, another work with a medieval setting.

Later in 1980 Rohmer embarked on a second series of films: the "Comedies and Proverbs", where each film was based on a proverb. The first "Comedy and proverb" was The Aviator's Wife, which was based on an idea that Rohmer had had since the mid-1940s. This was followed in 1981 with Le Beau Mariage (A Perfect Marriage), the second "Comedy and Proverb". Rohmer stated that "what interests me is to show how someone's imagination works. The fact that obsession can replace reality." In his review of the film, film critic Claude Baignères said that "Eric Rohmer is a virtuoso of the pen Sketch...[He had not been] at ease with the paint tubes that Persival required, [but in this film he created] a tiny figurine whose every feature, every curl, every tone is aimed at revealing to us a state of soul and of heart." Raphael Bassan said that "the filmmaker fails to achieve in these dialogues the flexibility, the textual freedom of The Aviator's Wife. A Perfect Marriage is only a variation on the spiritual states of the petty bourgeoise who go on and on forever about the legitimacy of certain institutions or beliefs confronted by problems of the emotions. Quite simply, this is a minor variation on this central Rohmerian theme."

The third "Comedy and proverb" was Pauline at the Beach in 1983. It won the Silver Bear for Best Director at the 33rd Berlin International Film Festival. It was based on an idea that Rohmer had in the 1950s, originally intended for Brigitte Bardot. Rohmer often made films that he had been working on his many years and stated "I can't say 'I make one film, then after that film I look for a subject and write on that subject...then I shoot.' Not at all...these are films that are drawn from one evolving mass, films that have been in my head for a long time and that I think about simultaneously."

The fourth "Comedy and Proverb" was Full Moon in Paris in 1984. The film's proverb was invented by Rohmer himself: "The one who has two wives loses his soul, the one who has two houses loses his mind." The film's Cinematographer Renato Berta called it "one of the most luxurious films ever made" because of the high amount of preparation put into it. The film began with Rohmer and the actors discussing their roles and reading from the film's scenario while tape recording the rehearsals. Rohmer then re-wrote the script based on these sessions and shot the film on Super 8mm as a dress rehearsal. When the film was finally shot, Rohmer often used between two and three takes for each shot, and sometimes only one take. Alain Bergala and Alain Philippon have stated that "all the art of Eric Rohmer consists of creating on the set avertable osmosis among himself, the actors and the technicians." Rohmer even encouraged Actress Pascale Ogier to design sets for the film since her character is an interior decorator. Ogier later won the Best Actress award at the Venice Film Festival. Alain Philippon called the film "one of the most accomplished films that Rohmer has given us...and that if the film moves it is because of its own risk-taking."

Rohmer saw the full-face closeup as a device that does not reflect how we see each other and avoided its use. He avoids extradiegetic music (not coming from onscreen sound sources), seeing it as a violation of the fourth wall. He has on occasion departed from the rule by inserting Soundtrack music in places in The Green Ray (1986) (released as Summer in the United States). Rohmer also tends to spend considerable time in his films showing his characters going from place to place, walking, driving, bicycling or commuting on a train, engaging the viewer in the idea that part of the day of each individual involves quotidian travel. This was most evident in Le Beau Mariage (1982), which had the female protagonist constantly traveling, particularly between Paris and Le Mans.

The Sixth "Comedy and Proverb" was Boyfriends and Girlfriends (L'Ami de mon amie) in 1987.

He followed these with a third series in the 1990s: Tales of the Four Seasons. Conte d’automne or Autumn Tale was a critically acclaimed release in 1999 when Rohmer was 79.

A Summer's Tale (1996) has most of the elements of a typical Rohmer film: no Soundtrack music, no closeups, a seaside resort, long conversations between beautiful young people (who are middle class and educated) and discussions involving the characters' interests from songwriting to ethnology.

Beginning in the 2000s, Rohmer, in his eighties, returned to period drama with The Lady and the Duke and Triple Agent. The Lady and the Duke caused considerable controversy in France, where its negative portrayal of the French Revolution led some critics to label it monarchist propaganda. Its innovative cinematic style and strong acting performances led it to be well received elsewhere.

The Venice Film Festival awarded Éric Rohmer the Career Golden Lion in 2001.

In 2007, Rohmer's final film, The Romance of Astrea and Celadon, was shown during the Venice Film Festival, at which he spoke of retiring.

On 8 February 2010, the Cinémathèque Française held a special tribute to Rohmer which included a screening of Claire's Knee and a short video tribute to Rohmer by Jean-Luc Godard.

The director's characters engage in long conversations—mostly talking about man-woman relationships but also on mundane issues like trying to find a vacation spot. There are also occasional digressions by the characters on literature and philosophy as most of Rohmer's characters are middle class and university educated.