Supergirl, vol. 4
Churchill's early work included stints on Supergirl, Uncanny X-Men as well as the Deadpool: Sins of the Past limited series, in addition to a lengthy stay on Cable, the latter gaining him (along with writer Jeph Loeb) fan acclaim. Loeb and Churchill were to later team up to produce Coven and Lionheart for Awesome Comics.
In 2009 Churchill drew the "Code Red" story arc in Hulk, which introduced the Red She-Hulk. The title, inked by Mark Farmer, saw a change in his usual drawing style, the result of a shoulder injury which required surgery.
In December 2010, Churchill's creator-owned comic "Marineman" launched to critical acclaim, securing an Eisner nomination for best new series 2010. The collected trade paperback of volume 1, "Marineman: A Matter of Life and Depth", was published in 2011. Churchill begins work on volume 2 of Marineman in 2013. Marineman, which Churchill writes and pencils and does the final colours, is published through Image Comics.
On April 9, 2011 Churchill was one of 62 comics creators who appeared at the IGN stage at the Kapow! convention in London to set two Guinness World Records, the Fastest Production of a Comic Book, and Most Contributors to a Comic Book. With Guinness officials on hand to monitor their progress, writer Mark Millar began work at 9am scripting a 20-page black and white Superior comic book, with Churchill and the other artists appearing on stage throughout the day to work on the pencils, inks, and lettering, including Dave Gibbons, Frank Quitely, John Romita Jr., Jock, Doug Braithwaite, Olivier Coipel, Duncan Fegredo, Simon Furman, David Lafuente, John McCrea, Sean Phillips and Liam Sharp, who all drew a panel each, with regular Superior artist Leinil Yu creating the book's front cover. The book was completed in 11 hours, 19 minutes, and 38 seconds, and was published through Icon on November 23, 2011, with all royalties being donated to Yorkhill Children's Foundation.
In 2012 Churchill was the artist on The Ravagers series for DC  and also mentored the wildly popular Image Comics title No Place Like Home. Volume 1 of Marineman was published in hardback format in French.
Comics work (interior pencil) art includes:
- Coven #1-6
- Coven, vol. 2, #1-3
- Coven Black & White
- Coven: Fantom
- Lionheart, miniseries, #1-2 (1999)
- Supreme: The Return #5 (2000)
- Adventures of Superman #639 (2005)
- Action Comics #826, 836 (among other artists) (2005–06)
- All-Flash #1 (among other artists) (2007)
- DCU Holiday Special (Aquaman) #1 (2009)
- The Ravagers #0-3, 5 (2012)
- Superman, vol. 2, #165 (among other artists), 176, 180, 216 (2001–05)
- Superman/Batman #19 (full art); #26, 50 (among other artists) (2005–08)
- Supergirl, vol. 4, #0-5, 7, 9, 10, 13-15 (2005–07)
- Titans East Special (2008)
- Titans #1 (2008)
- Marineman #1-6 (2010-2011)
- "Marineman: A Matter of Life and Depth" (2011)
- No Place Like Home (variant cover only) #1 (2012)
- "The Revenge" (2014 - Current)
- Avengers, vol. 2, #4-5, Annual 2001 (among other artists); #6-7 (full art) (1997)
- Cable #3 (among other artists); #20, 22-23, 25, 27, 29-35, 37-39 (1993–97)
- Captain America, vol. 2, #6 (along with Rob Liefeld) (1997)
- Deadpool, miniseries, #1-4 (1994)
- Excalibur #74 (1994)
- Hulk, vol. 3, #14-17 (2009)
- Uncanny X-Men #394-396, Annual #18 (1994-2001)
- Wolverine #80, 156-157 (1994-2000)
- X-Men, vol. 2, Annual #2 (1993)
- X-Men: The Wedding Album (1994)
- X-Men Chronicles #2 (1995)
- Cowsill, Alan; Dolan, Hannah, ed. (2010). "2000s". DC Comics Year By Year A Visual Chronicle. Dorling Kindersley. p. 321. ISBN 978-0-7566-6742-9.
Superman's cousin Kara Zor-El received her own title. Written by Jeph Loeb and illustrated by Ian Churchill, the fourth [ongoing] series featured a Supergirl still getting accustomed to her life on Earth
- Phegley, Kiel (October 2, 2009). "Inside Ian Churchill's New Style". Comic Book Resources. Retrieved March 21, 2010.
- "Kapow! '11: Comic History Rewritten On The IGN Stage". IGN. April 14, 2011
- "Guinness World Records at Kapow! Comic Con". Guinness World Records. April 9, 2011
- Kushins, Josh (January 12, 2012). "DC Comics in 2012-–-Introducing the "Second Wave" of DC Comics The New 52". The Source. DC Comics. Archived from the original on January 14, 2012. Retrieved January 14, 2012.
- Johnston, Rich (2 September 2013). "Jonathan Ross And Ian Churchill’s The Revenger – A New Comic For 2014". DC Comics. Retrieved 8 November 2013.