After the return of the RDA to Pandora and the deployment of the Recombinant unit to hunt Jake Sully, Spider became of special interest to the RDA due to his connection to the Sully family- and to Colonel Miles Quaritch. Taken captive by the Recombinants, Quaritch forced Spider to accompany them on their reconnaissance and teach the Recombiants to navigate Pandora like natives. Through the unorthodox bonding experience, Spider developed conflicted feelings towards Quaritch, the man that fathered him.

During the Battle at the Cove of the Ancestors, Spider escaped RDA captivity by sabotaging the Sea Dragon’s controls and wrecking the vehicle. He joined the Sully children and Tsireya, who were also imprisoned on the ship, before making a daring escape through the ship’s moon pool. The eldest Sully, Neteyam, was grievously wounded in the escape, and Spider was forced to watch helplessly as Neteyam died in Jake’s arms on the reef.

With the threat to Kiri and Tuktirey still present, Jake Sully relied on Spider’s intimate knowledge of the RDA’s ship to stage a counterassault- sneaking onto the ship and tearing through the Recombinant squad to get to his children. In a tense showdown between Quaritch - holding Kiri hostage at knifepoint - and Netytiri, Spider was used as leverage when he was similarly taken hostage by an infuriated Neytiri. Ultimately, Quaritch relented, releasing Kiri, Tuktirey and Spider to escape with the Sully family. The conflict wasn’t over, however, as Jake engaged Quaritch in hand-to-hand combat - determined to protect his family once and for all. Forced back onto the ship by an oil fire, Spider, Kiri, Neytiri and Tuktirey were separated again as the vessel began to rapidly sink.

From atop the bow of the overturned ship, Spider and Kiri both resolved to help their trapped family. Spider dove below the waves in search of the Sullys, but was startled to find the drowning body of his father at the bottom of the ocean. In a moment of exasperation, Spider chose to drag Quaritch to safety before abandoning him and returning to the Sully family.

Wounded, beaten, but alive, Spider and the Sully family recovered and mourned the death of Neteyam among the Metkayina people. Together, they attempted to return to some sense of normalcy, each grieving in their own way. The stillness did not last long, however, as a close call with Spider’s exo-pack frightened Jake for Spider’s well-being at the Metkayina Village, so far from other humans at High Camp. Deciding to return Spider to the High Camp outpost, the Sully family traveled with the Tlalim clan en route back to the Hallelujah Mountains.

Their journey was interrupted by Mangkwan raiders, who fell upon the convoy in fury, trailing smoke and raining destruction. Separated during the skirmish and forced to flee, Spider and the Sully children were pursued through the forest by the Mangkwan. Alone and on the run, one problem led to another as Spider’s exo-pack failed again, with no back up unit available. Desperate for her friend, Kiri Sully cried out to Eywa for help and tapped the neural network of the forest to save Spider- altering his biology and enabling him to breathe Pandoran air without the need of an exo-pack.

This development shocked Jake and Neytiri, presenting a new, dire threat to the Na’vi people were the RDA to capture Spider and learn how to reverse-engineer Kiri’s miracle. To make matters worse, Quaritch himself witnessed the boy’s new ability, meaning the RDA would certainly redouble their effort to locate him. Jake and Neytiri argued over how to respond, before ultimately Jake decided to return Spider to the reef where he will be hidden far from the RDA. Quaritch, however, had other plans.

Joining forces with the Mangkwan, Quaritch and his newfound allies returned to the reef, capturing both Spider and Jake Sully. The two were returned to Bridgehead- Spider for study and Jake for execution. Unwittingly given the means to escape his cell by a visit from Quaritch, three separate plans to save Jake collided as Neytiri, Spider, and a very anxious Dr. Ian Garvin each contributed to his freedom in their own way.

Beaten down and at a loss for direction, Jake realized the risk to the Na’vi people should the RDA be able to recreate Spider’s biological change while he was captured by them. He led Spider deep into the forest with the intent of sacrificing him to protect the Na’vi. Jake’s affection for Spider ultimately rendered him unable to follow through with the sacrifice, and together with Neytiri they resolved to find a different path to protect their people.

When the tide turned against the defenders in the Battle at the Cove of the Ancestors, Spider, Kiri and Tuktirey together petitioned Eywa to intervene - Spider himself lending Kiri the strength she needed to push through Eywa’s unexplained block and confront the entity face to face. As the tide of Pandoran fauna crashed against the RDA, Spider joined the fight, confronting Quaritch with Jake high above the cove inside the Flux Devil. In the chaos, Spider nearly slipped from atop a floating platform before being saved by both Jake and Quaritch, causing a truce. Before the battle could resume, Neytiri and Kiri arrived, and Quaritch leaped into the raging inferno below.

In the time after the battle, now finally able to connect to Eywa in her own right, Kiri guided Spider through the Pandoran neural network to find his place among the People, marking a brand-new era for Pandora.