It is widely acknowledged that opaque orthographies place additional demands on learning, often requiring many years to fully acquire. It is less widely recognized, however, that such opacity may offer certain benefits in the context of reading. For example, heterographic homophones such as ⟨knight⟩ and ⟨night⟩ (words that sound the same but which are spelled differently) impose additional costs in learning but reduce ambiguity in reading. Here, we consider the possibility that—left to evolve freely—writing systems will sometimes choose to forego some simplicity for the sake of informativeness when there is functional pressure to do so. We investigate this hypothesis by simulating the evolution of orthography as it is transmitted from one generation to the next, both with and without a communicative pressure for ambiguity avoidance. In addition, we consider two mechanisms by which informative heterography might be selected for: differentiation, in which new spellings are created to differentiate meaning (e.g., ⟨lite⟩ vs. ⟨light⟩), and conservation, in which heterography arises as a byproduct of sound change (e.g., ⟨meat⟩ vs. ⟨meet⟩). Under pressure from learning alone, orthographic systems become transparent, but when combined with communicative pressure, they tend to favor some additional informativeness. Nevertheless, our findings also suggest that, in the long term, simpler, transparent spellings may be preferred in the absence of top-down explicit teaching.