Scribblenauts is an exclusively side-scrolling game controlled almost entirely with the Nintendo DS stylus, with the D-pad and face buttons controlling the camera and the left and right shoulder buttons rotating objects. The player controls a character named Maxwell, who must collect objects called "Starites" to complete each level. Maxwell is guided by tapping the touchscreen, or if the player taps an object, Maxwell will pick it up or be given other options for interacting with that object, such as riding a horse or bicycle or shooting at an object if he holds a weapon. A fundamental element of Scribblenauts is the ability of the player to summon myriad objects into the game. This is achieved by writing the name of an object on the touchscreen. For example, the player can write "ladder", summoning a ladder, which the player may use to climb to an out-of-reach Starite. The player may turn the ladder on its side and set it on fire. The player may also chain objects together, such as chaining a piece of meat to a pole and holding it while riding on a raptor.
Summoned objects range among animals, weapons, forces of nature, famous people (both fictional and real), vehicles, household objects, easter eggs of the development team, and even internet memes. However, the game does not include trademarked terms, nor potential profanity (summoning "ass" will spawn a donkey; summoning "cock" will spawn a rooster). The game includes a homonym system to offer the player possible choices between similar-sounding objects, such as distinguishing between a toy balloon and a hot-air balloon; there is also a spellchecker to provide close matches for misspelled words. The North American release includes support for other languages including Brazilian Portuguese, French, and Spanish, with French-Canadian and Latin American variants available for words in the French and Spanish language sets, respectively. The UK version also accounts for difference between American and British English, such as the differing meanings of the word "football". 5th Cell has stated that the limit to what objects may be summoned is up to the player's imagination. Players, using special software, claimed to have discovered that the full list of words is greater than 22,800 unique entries, but, in response, Slaczka said there were many more than this number.
The game is segmented into 220 levels over 10 themed areas, and each given a 4 star ranking based on its difficulty, with later areas featuring more high ranked levels. Puzzles are given a par for the number of objects they can summon, typically being between two and four, though the player is free to summon more, so long as there is space in the meter at the top screen (summoning the same number of objects as the par or less earns more points). There are two types of levels—puzzle and action levels. Puzzle levels are real-life situations (such as having to open a piñata) where the Starite is awarded once the puzzle is solved, while action levels will appeal to gamers that prefer side-scrolling platformers, featuring switches, spike traps, and other similar elements. Players are awarded "merits" for completing levels while meeting certain requirements, such as not summoning any weapon-like object. Once the player completes a level, a silver star appears on the level selection button and a "Free play" mode is unlocked. At that point, the player is given the option to play through the level three consecutive times without reusing objects. Successfully completing the challenge grants the player a gold star for that level. Scribblenauts presents a simplistic storyline, as the developers wished to focus on engaging gameplay. The game always rewards the player with "Ollars", its in-game money, to allow them to purchase new areas, different avatars and other visual changes to the game.
The game includes a level editor, allowing users to share these levels over the Nintendo Wi-Fi system. The player can start with any level that they have already beaten from the main game, and add new objects with new game properties. These new properties can vary significantly from the normal behavior, such as having a bear able to eat a plane.