Ireton was initially a moderate. At the Putney Debates he opposed extremism, disliked the views of the Republicans and the Levellers, which he considered impractical and dangerous to the foundations of society, and wished to retain the constitution of King, Lords and Commons. He argued for these in the negotiations of the army with Parliament, and in the conferences with the king, being the person chiefly entrusted with the drawing up of the army proposals, including the manifesto called "The Heads of the Proposals" which proposed a constitutional monarchy. He tried to prevent the breach between the army and parliament, but when it happened, he supported the negotiations with the king until his actions made him unpopular.

Ireton finally became convinced of the hopelessness of dealing with King Charles, and, after the king's flight to the Isle of Wight, treated his further proposals with coldness and urged the parliament to establish an administration without him. Ireton served under Thomas Fairfax in the second civil war in the campaigns, in Kent and Essex, although it was Fairfax, as Lord General, and not Ireton as is sometimes believed, who was responsible for the executions of Sir Charles Lucas and Sir George Lisle at Colchester. After the rejection by the king of the last offers of the army, Ireton zealously supported bringing him to trial. He wrote the Army's statement about the regicide—the Remonstrance of the Army—with Hugh Peters. He was active in the choice to purge rather than reelect Parliament and supported the second Leveller Agreement of the People. He sat on the king's trial and was one of the commissioners who signed the death warrant.