diff --git a/DESCRIPTION b/DESCRIPTION
index 61e3f2742..5cd7f4944 100644
--- a/DESCRIPTION
+++ b/DESCRIPTION
@@ -17,10 +17,10 @@ Description: Generate an attractive and useful website from a source
 License: MIT + file LICENSE
 URL: https://pkgdown.r-lib.org, https://github.com/r-lib/pkgdown
 BugReports: https://github.com/r-lib/pkgdown/issues
-Depends: 
+Depends:
     R (>= 3.6)
-Imports: 
-    bslib (>= 0.3.1),
+Imports:
+    bslib (>= 0.5.1),
     callr (>= 3.7.3),
     cli (>= 3.6.1),
     desc (>= 1.4.0),
@@ -40,7 +40,7 @@ Imports:
     withr (>= 2.4.3),
     xml2 (>= 1.3.1),
     yaml
-Suggests: 
+Suggests:
     covr,
     diffviewer,
     evaluate,
@@ -59,7 +59,7 @@ Suggests:
     sass,
     testthat (>= 3.1.3),
     tools
-VignetteBuilder: 
+VignetteBuilder:
     knitr
 Config/Needs/website: usethis, servr
 Config/potools/style: explicit
diff --git a/NEWS.md b/NEWS.md
index 4ad061cfa..19f03ab42 100644
--- a/NEWS.md
+++ b/NEWS.md
@@ -20,6 +20,7 @@
 * Fix setting `seed` in `build_reference()`. The seed was reset too early, before. (@salim-b, #2355)
 * Translates citation sections (@eliocamp, #2410).
 * Topic names that conflict with selector functions can now be listed as references in `_pkgdown.yml` (@dmurdoch, #2397).
+* pkgdown is now compatible with (and requires) bslib >= 0.5.1 (@gadenbuie, #2395).
 
 # pkgdown 2.0.7
 
diff --git a/R/navbar.R b/R/navbar.R
index 4b67ed012..e5d670332 100644
--- a/R/navbar.R
+++ b/R/navbar.R
@@ -5,7 +5,7 @@ data_navbar <- function(pkg = ".", depth = 0L) {
 
   style <- navbar_style(
     navbar = navbar,
-    theme = get_bootswatch_theme(pkg),
+    theme = get_bslib_theme(pkg),
     bs_version = pkg$bs_version
   )
 
@@ -21,7 +21,7 @@ navbar_style <- function(navbar = list(), theme = "_default", bs_version = 3) {
     list(type = navbar$type %||% "default")
   } else {
     # bg is usually light, dark, or primary, but can use any .bg-*
-    bg <- navbar$bg %||% bootswatch_bg[[theme]]
+    bg <- navbar$bg %||% purrr::pluck(bootswatch_bg, theme, .default = "light")
     type <- navbar$type %||% if (bg == "light") "light" else "dark"
 
     list(bg = bg, type = type)
diff --git a/R/package.R b/R/package.R
index dc7b5396a..95a978143 100644
--- a/R/package.R
+++ b/R/package.R
@@ -24,9 +24,11 @@ as_pkgdown <- function(pkg = ".", override = list()) {
   meta <- read_meta(pkg)
   meta <- modify_list(meta, override)
 
+  bs_version <- get_bootstrap_version(list(meta = meta))
+
   template_config <- find_template_config(
     package = meta$template$package,
-    bs_version = meta$template$bootstrap
+    bs_version = bs_version
   )
   meta <- modify_list(template_config, meta)
 
@@ -38,8 +40,6 @@ as_pkgdown <- function(pkg = ".", override = list()) {
   package <- desc$get_field("Package")
   version <- desc$get_field("Version")
 
-  bs_version <- check_bootstrap_version(meta$template$bootstrap, pkg)
-
   development <- meta_development(meta, version, bs_version)
 
   if (is.null(meta$destination)) {
@@ -98,6 +98,28 @@ read_desc <- function(path = ".") {
   desc::description$new(path)
 }
 
+get_bootstrap_version <- function(pkg) {
+  template_bootstrap <- pkg$meta[["template"]]$bootstrap
+  template_bslib <- pkg$meta[["template"]]$bslib$version
+
+  if (!is.null(template_bootstrap) && !is.null(template_bslib)) {
+    cli::cli_abort(
+      c(
+        sprintf(
+          "Both {.field %s} and {.field %s} are set.",
+          pkgdown_field(pkg, c("template", "bootstrap")),
+          pkgdown_field(pkg, c("template", "bslib", "version"))
+        ),
+        x = "Remove one of them from {.file {pkgdown_config_relpath(pkg)}}"
+      ),
+      call = caller_env()
+    )
+  }
+
+  version <- template_bootstrap %||% template_bslib
+  check_bootstrap_version(version, pkg)
+}
+
 check_bootstrap_version <- function(version, pkg) {
   if (is.null(version)) {
     3
diff --git a/R/theme.R b/R/theme.R
index 4d0c780c4..67fc1743b 100644
--- a/R/theme.R
+++ b/R/theme.R
@@ -34,14 +34,12 @@ data_deps_path <- function(pkg) {
 bs_theme <- function(pkg = ".") {
   pkg <- as_pkgdown(pkg)
 
-  theme <- get_bootswatch_theme(pkg)
-  theme <- check_bootswatch_theme(theme, pkg$bs_version, pkg)
+  bs_theme_args <- pkg$meta$template$bslib %||% list()
+  bs_theme_args[["version"]] <- pkg$bs_version
+  bs_theme_args[["preset"]] <- get_bslib_theme(pkg)
+
+  bs_theme <- exec(bslib::bs_theme, !!!bs_theme_args)
 
-  bs_theme <- exec(bslib::bs_theme,
-    version = pkg$bs_version,
-    bootswatch = theme,
-    !!!pkg$meta$template$bslib
-  )
   # Drop bs3 compat files added for shiny/RMarkdown
   bs_theme <- bslib::bs_remove(bs_theme, "bs3compat")
 
@@ -92,30 +90,54 @@ highlight_styles <- function() {
   path_ext_remove(path_file(paths))
 }
 
-get_bootswatch_theme <- function(pkg) {
-  pkg$meta[["template"]]$bootswatch %||%
-    pkg$meta[["template"]]$params$bootswatch %||%
-    "_default"
+get_bslib_theme <- function(pkg) {
+  preset <- pkg$meta[["template"]]$bslib$preset
+
+  if (!is.null(preset)) {
+    check_bslib_theme(preset, pkg, c("template", "bslib", "preset"))
+    return(preset)
+  }
+
+  bootswatch <-
+    pkg$meta[["template"]]$bootswatch %||%
+    # Historically (< 0.2.0), bootswatch wasn't a top-level template field
+    pkg$meta[["template"]]$params$bootswatch
+
+  if (!is.null(bootswatch)) {
+    check_bslib_theme(bootswatch, pkg, c("template", "bootswatch"))
+    return(bootswatch)
+  }
+
+  "default"
 }
 
-check_bootswatch_theme <- function(bootswatch_theme, bs_version, pkg) {
-  if (bootswatch_theme == "_default") {
-    NULL
-  } else if (bootswatch_theme %in% bslib::bootswatch_themes(bs_version)) {
-    bootswatch_theme
-  } else {
-    cli::cli_abort(c(
-      sprintf(
-        "Can't find Bootswatch theme {.val %s} ({.field %s}) for Bootstrap version {.val %s} ({.field %s}).",
-        bootswatch_theme,
-        pkgdown_field(pkg, c("template", "bootswatch")),
-        bs_version,
-        pkgdown_field(pkg, c("template", "bootstrap"))
-      ),
-      x = "Edit settings in {pkgdown_config_href({pkg$src_path})}"
-    ), call = caller_env())
+check_bslib_theme <- function(theme, pkg, field = c("template", "bootswatch"), bs_version = pkg$bs_version) {
+  if (theme %in% c("_default", "default")) {
+    return("default")
+  }
+
+  bslib_themes <- c(
+    bslib::bootswatch_themes(bs_version),
+    bslib::builtin_themes(bs_version),
+    # bs_theme() recognizes both below as bare bootstrap
+    "default",
+    "bootstrap"
+  )
+
+  if (theme %in% bslib_themes) {
+    return(theme)
   }
 
+  cli::cli_abort(c(
+    sprintf(
+      "Can't find Bootswatch or bslib theme preset {.val %s} ({.field %s}) for Bootstrap version {.val %s} ({.field %s}).",
+      theme,
+      pkgdown_field(pkg, field),
+      bs_version,
+      pkgdown_field(pkg, c("template", "bootstrap"))
+    ),
+    x = "Edit settings in {pkgdown_config_href({pkg$src_path})}"
+  ), call = caller_env())
 }
 
 bs_theme_deps_suppress <- function(deps = list()) {
diff --git a/tests/testthat/_snaps/render.md b/tests/testthat/_snaps/render.md
index d9ddfc5f3..3fe6c6d9a 100644
--- a/tests/testthat/_snaps/render.md
+++ b/tests/testthat/_snaps/render.md
@@ -1,6 +1,11 @@
-# check_bootswatch_theme() works
+# check_bslib_theme() works
 
-    Can't find Bootswatch theme "paper" (template.bootswatch) for Bootstrap version "4" (template.bootstrap).
+    Can't find Bootswatch or bslib theme preset "paper" (template.bootswatch) for Bootstrap version "4" (template.bootstrap).
+    x Edit settings in _pkgdown.yml
+
+---
+
+    Can't find Bootswatch or bslib theme preset "paper" (template.preset) for Bootstrap version "4" (template.bootstrap).
     x Edit settings in _pkgdown.yml
 
 # capture data_template()
diff --git a/tests/testthat/test-render.R b/tests/testthat/test-render.R
index fe6d98043..e77fe6c28 100644
--- a/tests/testthat/test-render.R
+++ b/tests/testthat/test-render.R
@@ -1,8 +1,33 @@
-test_that("check_bootswatch_theme() works", {
+test_that("check_bslib_theme() works", {
   pkg <- as_pkgdown(test_path("assets/reference"))
-  expect_equal(check_bootswatch_theme("_default", 4, pkg), NULL)
-  expect_equal(check_bootswatch_theme("lux", 4, pkg), "lux")
-  expect_snapshot_error(check_bootswatch_theme("paper", 4, pkg))
+  expect_equal(check_bslib_theme("_default", pkg, bs_version = 4), "default")
+  expect_equal(check_bslib_theme("lux", pkg, bs_version = 4), "lux")
+  expect_snapshot_error(check_bslib_theme("paper", pkg, bs_version = 4))
+  expect_snapshot_error(check_bslib_theme("paper", pkg, bs_version = 4, field = c("template", "preset")))
+})
+
+test_that("get_bslib_theme() works with template.bslib.preset", {
+  pkg <- local_pkgdown_site(test_path("assets/site-empty"), '
+    template:
+      bootstrap: 5
+      bslib:
+        preset: shiny
+        enable-shadows: true
+  ')
+
+  expect_equal(get_bslib_theme(pkg), "shiny")
+  expect_no_error(bs_theme(pkg))
+
+  pkg <- local_pkgdown_site(test_path("assets/site-empty"), '
+    template:
+      bootstrap: 5
+      bslib:
+        preset: lux
+        enable-shadows: true
+  ')
+
+  expect_equal(get_bslib_theme(pkg), "lux")
+  expect_no_error(bs_theme(pkg))
 })
 
 test_that("capture data_template()", {
diff --git a/vignettes/customise.Rmd b/vignettes/customise.Rmd
index c192bb50e..48b56c484 100644
--- a/vignettes/customise.Rmd
+++ b/vignettes/customise.Rmd
@@ -40,7 +40,7 @@ Upgrading to Bootstrap 5 has a low chance of breaking your site unless you were
 
 ## Theming
 
-There are two ways to change the visual style of your site from `_pkgdown.yml`: using a pre-packaged bootswatch theme or customising theme variables with bslib.
+There are two ways to change the visual style of your site from `_pkgdown.yml`: using a pre-packaged bootswatch theme or customising theme variables with [bslib](https://rstudio.github.io/bslib/).
 The following sections show you how.
 
 ### Bootswatch themes
@@ -56,13 +56,14 @@ template:
 Changing the bootswatch theme affects both the HTML (via the navbar, more on that below) and the CSS, so you'll need to re-build your complete site with `build_site()` to fully appreciate the changes.
 While you're experimenting, you can speed things up by just rebuilding the home page and the CSS by running `build_home_index(); init_site()` (and then refreshing the browser).
 
-Bootswatch templates with tall navbars (e.g. lux, pulse) also require that you set the `pkgdown-nav-height` bslib variable:
+Bootswatch templates with tall navbars (e.g. lux, pulse) also require that you set the `pkgdown-nav-height` bslib variable.
+Because Bootswatch themes are provided by the [bslib](https://rstudio.github.io/bslib/) R package, you can also nest the `bootswatch` field under the `bslib` field.
 
 ``` yaml
 template:
   bootstrap: 5
-  bootswatch: lux
   bslib:
+    bootswatch: lux
     pkgdown-nav-height: 100px
 ```
 
@@ -108,6 +109,19 @@ template:
 
 While iterating on colours and other variables you only need to rerun `init_site()` and refresh your browser; when iterating on fonts, you'll need to run `build_home_index(); init_site()`.
 
+Theming with bslib is powered by `bslib::bs_theme()` and the `bslib` field is a direct translation of the arguments to that function.
+As a result, you can fully specify a bslib theme using the `template.bslib` field, making it easy to share YAML with the `output.html_document.theme` field [of an R Markdown document](https://rstudio.github.io/bslib/articles/theming/index.html).
+
+``` yaml
+template:
+  bslib:
+    version: 5
+    bootswatch: lux
+    base_font: {google: "Roboto"}
+    heading_font: {google: "Roboto Slab"}
+    code_font: {google: "JetBrains Mono"}
+```
+
 ### Syntax highlighting
 
 The colours used for syntax highlighting in code blocks are controlled by the `theme` setting: