diff --git a/guix/inferior.scm b/guix/inferior.scm
index 680fe6a805b..1440c684ccd 100644
--- a/guix/inferior.scm
+++ b/guix/inferior.scm
@@ -1,5 +1,5 @@
 ;;; GNU Guix --- Functional package management for GNU
-;;; Copyright © 2018-2024 Ludovic Courtès <ludo@gnu.org>
+;;; Copyright © 2018-2025 Ludovic Courtès <ludo@gnu.org>
 ;;;
 ;;; This file is part of GNU Guix.
 ;;;
@@ -860,9 +860,13 @@ failing when GUIX is too old and lacks the 'guix repl' command."
 ;;;
 
 (define %inferior-cache-directory
-  ;; Directory for cached inferiors (GC roots).
-  (make-parameter (string-append (cache-directory #:ensure? #f)
-                                 "/inferiors")))
+  ;; Directory for cached inferiors (GC roots).  It must be world-readable so
+  ;; the daemon can traverse it.
+  (make-parameter (string-append %profile-directory "/inferiors")))
+
+(define %legacy-inferior-cache-directory
+  ;; Former directory for cached inferiors, by default under $HOME/.cache.
+  (string-append (cache-directory #:ensure? #f) "/inferiors"))
 
 (define* (channel-full-commit channel #:key (verify-certificate? #t))
   "Return the commit designated by CHANNEL as quickly as possible.  If
@@ -950,6 +954,14 @@ X.509 host certificate; otherwise, warn about the problem and keep going."
                                       #:entry-expiration
                                       (file-expiration-time ttl))
 
+  ;; Clean the legacy cache directory as well.  Remove this call once at least
+  ;; one year has passed.
+  (maybe-remove-expired-cache-entries %legacy-inferior-cache-directory
+                                      cache-entries
+                                      #:entry-expiration
+                                      (file-expiration-time ttl))
+
+
   (if (file-exists? cached)
       cached
       (run-with-store store
diff --git a/guix/scripts/environment.scm b/guix/scripts/environment.scm
index 41353e33053..15b84afb7fd 100644
--- a/guix/scripts/environment.scm
+++ b/guix/scripts/environment.scm
@@ -793,11 +793,24 @@ WHILE-LIST."
 
   (define (nesting-mappings)
     ;; Files shared with the host when enabling nesting.
+
+    ;; Make sure these two directories exist so they can be shared.
+    (mkdir-p (string-append %profile-directory "/profiles"))
+    (mkdir-p (string-append %profile-directory "/inferiors"))
+
     (cons* (file-system-mapping
             (source (%store-prefix))
             (target source))
            (file-system-mapping
-            (source (cache-directory))
+            (source (cache-directory))           ;~/.cache/guix/checkouts etc.
+            (target source)
+            (writable? #t))
+           (file-system-mapping                  ;'guix shell' cached GC roots
+            (source (string-append %profile-directory "/profiles"))
+            (target source)
+            (writable? #t))
+           (file-system-mapping           ;'guix time-machine' cached GC roots
+            (source (string-append %profile-directory "/inferiors"))
             (target source)
             (writable? #t))
            (let ((uri (string->uri (%daemon-socket-uri))))
diff --git a/guix/scripts/shell.scm b/guix/scripts/shell.scm
index d23362a15d5..80251606a32 100644
--- a/guix/scripts/shell.scm
+++ b/guix/scripts/shell.scm
@@ -1,5 +1,5 @@
 ;;; GNU Guix --- Functional package management for GNU
-;;; Copyright © 2021-2024 Ludovic Courtès <ludo@gnu.org>
+;;; Copyright © 2021-2025 Ludovic Courtès <ludo@gnu.org>
 ;;; Copyright © 2023 Janneke Nieuwenhuizen <janneke@gnu.org>
 ;;;
 ;;; This file is part of GNU Guix.
@@ -327,10 +327,13 @@ echo ~a >> ~a
 ;;;
 
 (define %profile-cache-directory
-  ;; Directory where profiles created by 'guix shell' alone (without extra
-  ;; options) are cached.
-  (make-parameter (string-append (cache-directory #:ensure? #f)
-                                 "/profiles")))
+  ;; Directory where profiles (GC roots) created by 'guix shell' are cached.
+  ;; It must be world-readable so the daemon can traverse it.
+  (make-parameter (string-append %profile-directory "/profiles")))
+
+(define %legacy-cache-directory
+  ;; Former cache directory, by default under $HOME/.cache.
+  (string-append (cache-directory #:ensure? #f) "/profiles"))
 
 (define (profile-cache-primary-key)
   "Return the \"primary key\" used when computing keys for the profile cache.
@@ -592,6 +595,13 @@ to make sure your shell does not clobber environment variables."))) )
                  (maybe-remove-expired-cache-entries
                   (%profile-cache-directory)
                   cache-entries
+                  #:entry-expiration entry-expiration)
+
+                 ;; Clean the legacy cache directory as well.  Remove this
+                 ;; call once at least one year has passed.
+                 (maybe-remove-expired-cache-entries
+                  %legacy-cache-directory
+                  cache-entries
                   #:entry-expiration entry-expiration)))
 
     (if (assoc-ref opts 'export-manifest?)