- “Diplomatic Orders”: In 2409, the Kirk joins the U.S.S. Challenger, U.S.S. Rideout, U.S.S. Terev, and U.S.S. Texas into the P'Jem System to engage an Undine Tethys Bio-Dreadnought threatening the player.
- “City on the Edge of Never”: B'vat's forces ambush and board the Kirk in the JFS47 System to capture Miral Paris.
- “Devil's Choice” & “Shadow Play”: The Kirk is part of Battlegroup Phi forming at Virinat in order to subsequently proceed to New Romulus. Here she joins with a joint Starfleet/KDF fleet assisting the Romulan Republic in defending New Romulus against an Elachi invasion fleet.
- “Blood of Ancients” & “Delta Flight”: In 2410, the Kirk is badly damaged during the battle against the Heralds at Lae'nas III. While being in drydock for subsequent repairs, many of her crew, including Lt. Cmdr. Paris, are temporarily reassigned to other ships.
- "Season 5 Dev Blog #6": The Kirk discovers an abandoned Jem'Hadar Attack Ship in the Pi Canis Sector Block.
- The U.S.S. Kirk was probably named after legendary Starfleet Captain James T. Kirk.
- Beginning in the Season 8.5-revamp of "City on the Edge of Never", a mysterious "Visitor" wearing the outfit of a Temporal Agent could be found in one of the turbolifts adjacent to the Kirk's bridge. With the release of Agents of Yesterday, this was revealed to be Barrett.
- Up until April 2012, the Kirk was a random Federation Cruiser class.
- In the "Chasing the Past" segment of “City on the Edge of Never” and in the final part of “Diplomatic Orders”, the Kirk is mislabeled U.S.S. Exeter.