Long Interspersed Element 1 (LINE-1 or L1) is a retrotransposon presently active in mammalian genomes. L1 insertions within and proximal to genes can impact gene expression in a variety of ways, and retrotransposition events are frequently associated with duplication, deletion, and rearrangement of genomic sequences. In order to exert an ongoing impact on genome evolution, new L1 insertions must occur in cells that will contribute their genetic material to subsequent generations—ie, within the germ lineage or in the pluripotent cells of the early embryo, prior to germline specification. Previous studies have suggested that the early embryo is a prominent milieu for L1 retrotransposition; however, systematic study of the frequency and developmental timing of heritable L1 retrotransposition events has been technically challenging. Here, we have adapted retrotransposon capture sequencing (RC-seq) to detect retrotransposon insertions in mouse genomes, and applied this technique to identify de novo heritable L1 insertions in multi-generation pedigrees of C57BL/6 mice. We identify 11 full-length Tf subfamily L1 insertions among 85 mouse genomes, providing a conservative estimate of 1 new inseriton per 8 mice. Using a PCR genotyping strategy to deduce developmental timing of these events, we find evidence consistent with L1 retrotransposition in the early embryo resulting in somatic and germline genetic mosaicism, as well as in early primordial germ cells (PGCs), giving rise to germline-restricted genetic mosaicism. We also identify L1 insertions attributable to later germline development. Furthermore, by exploiting 3’ transductions carried by two de novo insertions, we identify progenitor L1 elements active in the early primordial germline and in the pluripotent cells of the early embryo. Our findings shed new light on the frequency and developmental origins of the ongoing retrotransposition events continuously shaping mammalian genomes.