Abstract Transposable elements including LINE-1 (Long INterspersed Element-1) impact genome variation, function, regulation, and disease. LINE-1s seem to have expanded as distinct consecutive lineages, but the drivers of lineage emergence and disappearance are unknown. Reference genomes provide a snapshot of LINE-1 evolution; however, the ongoing retrotransposition of LINE-1s in humans is not evident in these mosaic assemblies. Utilizing long-read-based haploid assemblies, we identified the sequence and location of all the youngest LINE-1s in these genomes at allelic resolution. We cloned and assayed the in vitro retrotransposition activity of the subset of LINE-1s with intact open reading frames and found 34 were measurably active. Yet, among individuals, these same LINE-1s varied in their presence, allelic sequences, and activity. Using a measure of in vivo retrotransposition of closely related groups of LINE-1, we found that recently retrotransposed LINE-1s tend to be active in vitro and polymorphic in the population. However, for a considerable number of LINE-1s, their measured in vitro activity and inferred in vivo fitness were uncorrelated, regardless of their frequency in the population. Some of these unexpected patterns come from rare allelic forms of old LINE-1s that retain activity, suggesting older LINE-1 lineages can persist much longer than expected. Finally, some LINE-1s showed mutations that were potentially adaptive, increasing their replication in the genome. These key mutations specific to LINE-1s with both in vitro activity and in vivo fitness represent promising candidates for the future mechanistic investigation of the drivers of LINE-1 evolution which may contribute to disease susceptibility.