Ponnelle was born in Paris. He studied philosophy, art, and history there and, in 1952, began his career in Germany as a theatre designer for Hans Werner Henze's opera Boulevard Solitude. He was greatly influenced by the work of art director Georges Wakhévitch who also designed sets and costumes for the theatre, the ballet, and the opera.
In 1962, Ponnelle directed his first production of Richard Wagner's Tristan und Isolde in Düsseldorf. His production of that opera at the Bayreuth Festival in 1981 was widely praised as one of the most aesthetically beautiful in its history.
His work throughout the world included stage productions at the Metropolitan Opera and the San Francisco Opera; productions for television (a Madama Butterfly in 1974 notable for performances by Mirella Freni and the young Plácido Domingo); and filmed versions of operas such as the well-known Karl Böhm-conducted The Marriage of Figaro. His 1969 production of Mozart's then neglected La Clemenza di Tito for Cologne helped re-establish this work in the repertory. Ponnelle also was a frequent guest at the Salzburg Festival.
Often, his productions were controversial. His 1986 Aida at Covent Garden, in which he replaced the usual ballet dancers with young boys, was soundly booed and never revived, though his earlier Don Pasquale at the same theatre had been a triumph, as were his interpretations of well-known works. 
He died in Munich, Germany in 1988 of a pulmonary embolism following a tragic fall into the orchestra pit during rehearsals for a production of Carmen with the Israel Philharmonic Orchestra under Zubin Mehta. His son is the orchestra conductor Pierre-Dominique Ponnelle and his nephew is Jean Pierre Danel.
- Hindemith: Cardillac. Conductor - Wolfgang Sawallisch, Bavarian State Opera and Chorus. Singers: Donald McIntyre, Maria de Francesca-Cavazza, Robert Schunk, Hans Günter Nöcker. DVD: DGG 0044 007 3432 4
- Massenet: Manon ♦ (IMSLP). Conductor - Ádám Fischer, Chor und Orchestre der Wiener Staatsoper. Singers: Edita Gruberova, Francisco Araiza, Pierre Thau, Hans Helm. DVD: DGG 0440 073 4207 7
- Monteverdi: L'Orfeo ♦ (IMSLP). Conductor - Nikolaus Harnoncourt, Das Monteverdi-Ensemble des Opernhauses Zürich. Singers: Philippe Huttenlocher, Dietlinde Turban, Trudeliese Schmidt, Francisco Araiza, Christian Boesch. DVD: DGG 0440 073 4163 6
- Monteverdi: Il ritorno d'Ulisse in Patria ♦ (IMSLP). Conductor - Nikolaus Harnoncourt, Das Monteverdi-Ensemble des Opernhauses Zürich. Singers: Werner Hollweg, Trudeliese Schmidt, Francisco Araiza, Janet Perry. DVD: DGG 0440 073 4278 7
- Monteverdi: L'incoronazione di Poppea ♦ (IMSLP). Conductor - Nikolaus Harnoncourt, Das Monteverdi-Ensemble des Opernhauses Zürich. Singers: Rachel Yakar,Werner Hollweg, Trudeliese Schmidt, Paul Esswood. DVD: DGG 0440 073 4174 2
- Mozart: Mitridate, re di Ponto ♦ (IMSLP). Conductor - Nikolaus Harnoncourt, Concentus Musicus, Wien. Singers: Gösta Winbergh, Yvonne Kenny, Ann Murray, Anne Gjevang, Joan Rodgers, Peter Straka. DVD: DGG 0440 073 4127 8
- Mozart: Idomeneo ♦ (IMSLP). Conductor - James Levine, The Metropolitan Opera Orchestra and Chorus. Singers: Luciano Pavarotti, Ileana Cotrubas, Hildegard Behrens, Frederica von Stade, John Alexander. DVD: DGG 0440 073 4234 3 GH 2
- Mozart: Le Nozze di Figaro ♦ (IMSLP). Conductor - Karl Böhm, Vienna Philharmonic. Singers: Hermann Prey, Mirella Freni, Dietrich Fischer-Dieskau, Kiri Te Kanawa, Maria Ewing, Paolo Montarsolo. DVD: DGG 0440 073 4034 9
- Mozart: Così fan Tutte ♦ (IMSLP). Conductor - Nikolaus Harnoncourt, Vienna Philharmonic. Singers: Edita Gruberova, Delores Ziegler, Teresa Stratas, Luis Lima, Ferruccio Furlanetto, Paolo Montarsolo. DVD: DGG 0440 073 4237 4
- Mozart: Die Zauberflöte ♦ (IMSLP). Conductor - James Levine, Chor und Orchestre der Wiener Staatsoper. Singers: Ileana Cotrubas, Edita Gruberova, Peter Schreier, Walter Berry, Martti Talvela. DVD: ArtHaus 107 199
- Mozart: La Clemenza di Tito ♦ (IMSLP). Conductor - James Levine, Vienna Philharmonic. Singers: Tatiana Troyanos, Carol Neblett, Catherine Malfitano, Eric Tappy, Anne Howells, Kurt Rydl. DVD: DGG 0440 073 4128 5
- Orff: Carmina Burana (Original Source) ♦ Conductor - Kurt Eichhorn, Chor des Bayerischen Rundfunks & Münchner Rundfunkorchester. Singers: Lucia Popp, Hermann Prey, John van Kesteren. DVD: RCA 74321 852859 (Currently available in PAL format only)
- Puccini: Madama Butterfly ♦ (IMSLP). Conductor - Herbert Von Karajan, Wiener Philharmoniker. Singers: Mirella Freni, Plácido Domingo, Christa Ludwig, Robert Kerns, Michel Sénéchal. DVD: DGG 00440 073 4037
- Rossini: L'Italiana in Algeri ♦ (IMSLP). Conductor - James Levine, The Metropolitan Opera Orchestra and Chorus. Singers: Marilyn Horne, Paolo Montarsolo, [http://music.cmu.edu/people.php?sub_page=faculty&faculty_id=37 Douglas Ahlstedt, Allan Monk. DVD: DGG 0440 073 4261 9
- Rossini: Il Barbiere di Siviglia ♦ (IMSLP). Conductor - Claudio Abbado, Coro e Orchestra del Teatro alla Scala. Singers: Teresa Berganza ♦ (Official Website), Luigi Alva, Hermann Prey, Enzo Dara, Paolo Montarsolo. DVD: DGG 0440 073 4039 4
- Rossini: La Cenerentola ♦ (IMSLP). Conductor - Claudio Abbado, Coro e Orchestra del Teatro alla Scala. Singers: Frederica von Stade, Margherita Guglielmi, Laura Zannini, Francisco Araiza, Claudio Desderi, Paolo Montarsolo. DVD: DGG 0440 073 4096 7
- Verdi: Rigoletto ♦ (IMSLP). Conductor - Riccardo Chailly, Wiener Philharmoniker und Konzertvereinigung Wiener Staatsopernchor. Singers: Luciano Pavarotti, Ingvar Wixell, Edita Gruberova, Ferruccio Furlanetto. DVD: DGG 0440 073 4166 7
- Verdi: Falstaff ♦ (IMSLP). Conductor - Sir John Pritchard, London Philharmonic & Glyndebourne Chorus. Singers: Donald Gramm, Benjamin Luxon, Kay Griffel, Elizabeth Gale, Max René Cosotti, John Fryatt, Bernard Dickerson, Ugo Trama, Nucci Condo, Reni Penkova. DVD: Arthaus 101 083
- Wagner: Tristan und Isolde ♦ (IMSLP). Conductor - Daniel Barenboim, Orchester der Bayreuther Festspiele. Singers: René Kollo, Johanna Meier, Matti Salminen, Hermann Becht, Hanna Schwarz. DVD: DGG 0440 073 4321 0
- Salzbug Festival website (in English) Retrieved 3 January 2009
- Pfaff, San Francisco Chronicle: "Welcome as it may be to find Jean-Pierre Ponnelle's infamous 1975 Eurotrash production of the work, presented as "The Steersman's Dream", (which held the War Memorial stage for three of the company's five presentations of the piece) banished, presumably forever, it can still be a strain to discern Dutchman.
- Porter, Andrew, The Times: "Only in recent years have directors taken it upon themselves to rewrite Wagner's stage actions, to intervene, to move from simplification to new invention. Jean-Pierre Ponnelle's idea at Bayreuth, in 1981, was that Isolde should not appear in Act Three but be an off-stage voice sounding in Tristan's mind"
- Chatfield-Taylor, p. 63: "Some critics felt that there was...perversity in Ponnelle's conception of (Rigoletto) as a flashback that begins with Gilda already dead, lying on the floor during the Prelude".
- Chatfield-Taylor, Joan, San Francisco Opera: The First 75 Years, San Francisco: Chronicle Books, 1997, ISBN 0-8118-1368-1,
- Pfaff, Timothy, "Dutchman' Can't Quite Fly: Opera Cast Struggles With New Production of Wagner", San Francisco Chronilcle, 1 October 1997
- Porter, Andrew, "Lovers with extra trimmings", The Times (London) August 21, 1998
- John Rockwell, "Jean-Pierre Ponnelle, 56, Is Dead; Was Opera Director And Designer", New York Times, August 12, 1988
- "Grand Operator", The Guardian, (London), 13 August 1988 (Obituary)
- IMdB entry for Ponnelle listing major productions for film, TV, and stage