embed/Makefile.am        | 1 +
 embed/ephy-embed-shell.c | 1 +
 2 files changed, 2 insertions(+)

diff --git c/embed/Makefile.am i/embed/Makefile.am
index 8969e1b59e252c19..7c3225b02c2ec5fb 100644
--- c/embed/Makefile.am
+++ i/embed/Makefile.am
@@ -65,6 +65,7 @@ libephyembed_la_CPPFLAGS = \
 libephyembed_la_CFLAGS = \
 	-DDATADIR="\"$(datadir)\""	\
 	-DSHARE_DIR=\"$(pkgdatadir)\"	\
+	-DEPHY_PLUGINS_DIR=\""$(libdir)/epiphany/plugins"\" \
 	-DEPHY_WEB_EXTENSIONS_DIR=\""$(libdir)/epiphany/$(EPIPHANY_MAJOR)/web-extensions"\" \
 	$(DEPENDENCIES_CFLAGS) 	\
 	$(CODE_COVERAGE_CFLAGS) \
diff --git c/embed/ephy-embed-shell.c i/embed/ephy-embed-shell.c
index cd74f7d144b37ed3..624020f3c39383c6 100644
--- c/embed/ephy-embed-shell.c
+++ i/embed/ephy-embed-shell.c
@@ -671,6 +671,7 @@ ephy_embed_shell_create_web_context (EphyEmbedShell *shell)
   g_free (cache_dir);
 
   priv->web_context = webkit_web_context_new_with_website_data_manager (manager);
+  webkit_web_context_set_additional_plugins_directory (priv->web_context, EPHY_PLUGINS_DIR);
   g_object_unref (manager);
 }