He first appears in history in 426 BC in an invasion of Aetolia. The invasion was a failure and Demosthenes did not return to Athens, fearing for his life. Later that year, Ambracia invaded Acarnania, and the Acarnanians sought help from Demosthenes, who was now patrolling the coast of the Ionian Sea with twenty Athenian ships. He landed at Olpae and defeated a Spartan army under Eurylochus which had come to assist the Ambraciots. Demosthenes defeated Eurylochus (who was killed in the battle) and the Acarnanians and Ambraciots signed a peace treaty. See Battle of Olpae.
In 425 he was still patrolling the Ionian Sea, and was ordered to join with a fleet sent from Athens to put down a revolt in Sicily. Due to a storm, Demosthenes instead landed at Pylos in the Peloponnese. In order to keep his soldiers busy, he had them fortify the port, giving Athens a strong base close to Sparta. Sparta, meanwhile, landed an army on the nearby island of Sphacteria, and Demosthenes moved his men to the beach to prevent the Spartans, commanded by Brasidas, from landing there. The Spartan landing was repulsed, and the Athenian fleet (having turned back from their journey to Sicily) arrived to chase off the Spartan ships. Back in Athens, the Spartans tried to negotiate for peace; this failed, and Cleon was sent to assist Demosthenes, who was planning an invasion of Sphacteria. The two Athenians invaded and the Spartans uncharacteristically surrendered. See Battle of Pylos and Battle of Sphacteria.
In 424 Demosthenes and Hippocrates attempted to capture Megara, but they were defeatd by Brasidas. Demosthenes then went to Naupactus to assist in a democratic revolution, and to gather troops for an invasion of Boeotia. Demosthenes and Hippocrates were unable to coordinate their attacks and Hippocrates was defeated at the Battle of Delium. Demosthenes instead attacked Sicyon and was defeated as well. In 421 Demosthenes was one of the signatories of the Peace of Nicias which ended the first half of the war. (Another Demosthenes was also a signatory for Sparta.)
In 417 Demosthenes was responsible for evacuating the Athenian troops from Epidaurus following the Battle of Mantinea. He organized athletic games and the Athenian troops escaped while the Epidaurans were distracted.
In 415 Athens invaded Sicily. A Spartan fleet soon arrived to reinforce their allies in Syracuse, and a stalemate ensued. In 414 Demosthenes and Eurymedon were sent with a new fleet of seventy-three ships and 5000 hoplites. Demosthenes landed his troops and lead a bold night attack on Syracusan forces. After initial success, the Athenian troops became disorganized and soon very confused in the chaotic night operation, and were thouroughly routed by Gylippus, the Spartan commander. After the defeat, and upon seeing the disease-ridden Athenian camp, Demosthenes suggested that they immediately give up the siege and return to Athens, where they were needed to defend against a Spartan invasion of Attica. Nicias, the top Athenian commander, at first refused, until still more Spartans arrived. However, while preparing to leave there was a lunar eclipse, which delayed the departure as it was considered a bad omen. The Syracusans and Spartans trapped them in the harbour and Eurymedon was killed. The Spartans forced the Athenians to re-land their men. Demosthenes thought they could still flee by ship but Nicias wanted to find refuge on land. After a few days or marching Demosthenes and Nicias became separated; Demosthenes was ambushed by the Syracusans and was forced to surrender. Nicias was soon captured as well, and both were executed against the orders of Gylippus, who had hoped Demosthenes could be brought back to Sparta as a prisoner.
Demosthenes was also a character in The Knights by Aristophanes. Along with Nicias, he is a slave who overthrows "the Paphlagonian," a character representing Cleon. The characters were based on the real people, who were contemporaries of Aristophanes.