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Abstract AimTo determine the historical dynamics of colonization and whether the relative timing of colonization predicts diversification rate in the species‐rich, murine rodent communities of Indo‐Australia. LocationIndo‐Australian Archipelago including the Sunda shelf of continental Asia, Sahul shelf of continental Australia, the Philippines and Wallacea of Indonesia. TaxonOrder Rodentia, Family Muridae. MethodsWe used a fossil‐calibrated molecular phylogeny and Bayesian biogeographical modelling to infer the frequency and temporal sequence of biogeographical transitions among Sunda, Sahul, the Philippines and Wallacea. We estimated diversification rates for each colonizing lineage using a method‐of‐moments estimator of net diversification and Bayesian mixture model estimates of diversification rate shifts. ResultsWe identified 17 biogeographical transitions, including nine originating from Sunda, seven originating from Sulawesi and broader Wallacea and one originating from Sahul. Wallacea was colonized eight times, the Phillipines five times, Sunda twice and Sahul twice. Net diversification rates ranged from 0.2 to 2.12 species/lineage/My with higher rates in secondary and later colonizers than primary colonizers. The highest rates were in the genusRattusand their closest relatives, irrespective of colonization history. Main ConclusionsOur inferences from murines demonstrate once again the substantial role of islands as sources of species diversity in terrestrial vertebrates of the IAA with most speciation events occurring on islands. Sulawesi and broader Wallacea have been a major source of colonists for both island and continental systems. Crossings of Wallace's Line were more common than subsequent transitions across Lydekker's Line to the east. While speciation following colonization of oceanic archipelagos and large islands is consistent with adaptive radiation theory and ideas regarding ecological opportunity, we did not observe a strong signal of incumbency effects. Rather, subsequent colonists of landmasses radiated unhindered by previous radiations.