In addition to original versions of the games, Halo: The Master Chief collection will also include a new visually-upgraded version of Halo 2.
Purchasers of the November release are also being promised "beta" access to the multiplayer version of the forthcoming Halo 5.
One company watcher said it illustrated the firm was listening to its fans.
"I think it's a smart move," said David Scarborough, from GamesTM magazine.
"It shows a willingness to satiate the appetite of Xbox hardcore gamers, which is what Microsoft sees the Halo franchise as - it's biggest hardcore gaming franchise.
"It also feeds into the hype for the next entry in the series.
"But I personally don't think it will be something that will incentivise people who haven't yet bought a new console to buy an Xbox One."
Xbox gamers who already bought the titles on earlier versions of the Xbox are being given an added reason to buy the games again: the package will also include access to watch a new live-action series called Halo: Nightfall.
The episodes, produced by Ridley Scott, are currently being filmed in Ireland, and are separate to the Steven Spielberg Halo TV series promised last year.
While new pre-rendered trailer footage of Halo 5 was shown to the audience at the firm's E3 press conference in Los Angeles, developer 343 Studios was not yet ready to demo gameplay or confirm a launch date.
Xbox chief Phil Spencer told the crowd at the Microsoft event  that Halo was the "reason Xbox is here today".
He also acknowledged that his firm had changed its strategy to take account of customer feedback - a nod to it abandoning restrictions on the sale of second-hand disks and releasing a cheaper version of the console without its Kinect voice/camera sensor.
He pointedly said at the event's outset that this year's conference would be dedicated exclusively to showing off new games, rather than sharing the time to show off other multimedia features.
Microsoft's rival Sony had exploited previous attempts to promote the Xbox as both a games machine and a means to control cable TV, pitching the PlayStation 4 as the machine for serious gamers. That move helped the Japanese company to enjoy stronger sales since both machines launched last November.
Other new titles on show for the Xbox One included the hyper-reality game Sunset Overdrive, which features a character who skids across rails blowing up people who have been turned into mutants by a poisonous fizzy drink.
The colourful game is an Xbox One exclusive and due out later this year.
Microsoft Game Studios showed off another new Xbox One exclusive at an earlier stage of development called Phantom Dust - which is billed as a "battle for reality". It had previously released an action-strategy title by the same name for the original Xbox a decade ago.
The in-house games publisher also previewed a dragon-fighting title - developed by Japan's Platinum Games - called Scalebound for the new console, and a fresh version of its open-world third-person shooter Crackdown, originally released for the Xbox 360.
One expert said offering such distinctive titles could prove critical to Microsoft's attempts to woo those who had not yet upgraded to a "new-gen" console.
"Since Xbox dropped the DRM [digital rights management] stuff before launch and then ditched the Kinect as a must-have about a month ago, the actual level of differentiation between PlayStation 4 and Xbox One has really shrunk," said Ed Barton, an analyst at the Ovum consultancy.
"So, one of the only differentiators left is exclusive game titles - there's not much left in to pick between them based on hardware."
Analysis from E3: Dave Lee, Los Angeles
First stop at this year's E3 was the Galen Center, a venue usually used for basketball, where Microsoft rolled out its portfolio for the coming year and a bit.
At its heart, the crowd-pleasing announcement of the Halo Master Collection - a complete compendium of the Halo series, plus a "beta" of the latest entry in the series, Halo 5 Guardians. It won the biggest cheer in the arena, for mostly nostalgia purposes.
But a new console can't rely on old franchises, even if they are of Halo's calibre. That's where Sunset Overdrive comes in - an (almost) open-world game with a lead character that, at first glance, is more than slightly irritating.
While the Xbox event was a typically loud, brash affair - it was intentionally no-nonsense. This was all about games, and the firm has set out a convincing staple for the year ahead, even if it is a little reliant on tried and tested brands.
It all points to a strong 2014 and 2015 for Xbox One. It needs to be if it is to claw back some of the ground lost to the PlayStation 4.
Tellingly, there was only a brief mention of the Kinect - a peripheral touted last year to be integral to the Xbox One experience.
Not so this time - only two titles mentioned the Kinect directly: a dancing game and a baffling music-creation game based on the old Disney film, Fantasia.
Later we get to see what Sony has to offer.
Square Enix picked the show to premiere a trailer for its next Lara Croft game, called Rise of the Tomb Raider. The character appears to be suffering post-traumatic stress disorder after her previous origins story, but little of the new plot was revealed.
Activision was more forthcoming with a long sequence from its forthcoming Call of Duty: Advanced Warfare game, showing soldiers fighting swarms of drones in a battle-hit city. However, there was only a brief glimpse of its star Kevin Spacey in the footage.
Several titles on show took advantage of the Xbox's extra processing power to offer fast-paced multiplayer campaigns. They included:
Microsoft is recoding the main games in its Halo series to run on its recently released Xbox One console.